Review
Tansley review
Origin and domestication of Cucurbitaceae
crops: insights from phylogenies, genomics and
archaeology
Authors for correspondence:
Guillaume Chomicki
Email: guillaume.chomicki@gmail.com
Guillaume Chomicki1,2
, Hanno Schaefer3
and Susanne S. Renner4
1
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK; 2The Queen’s College, University of
Oxford, High St, Oxford, OX1 4AW, UK; 3Plant Biodiversity Research, Technical University of Munich, Emil-Ramann Str. 2,
Hanno Schaefer
Tel: +49 8161 71 5884
Email: hanno.schaefer@tum.de
Freising 85354, Germany; 4Systematic Botany and Mycology, University of Munich (LMU), Menzinger Str. 67, Munich 80638,
Germany
Received: 30 January 2019
Accepted: 17 May 2019
Contents
Summary
1
I.
Introduction
1
II.
The diversity of cultivated Cucurbitaceae: traits of major
and minor crops
2
Time and place of domestication
6
III.
IV. The genomics of Cucurbitaceae domestication
V.
Conclusions
13
Acknowledgements
13
References
13
11
Summary
New Phytologist (2019)
doi: 10.1111/nph.16015
Key words: cucumber, domestication,
genomics, melon, pumpkin, squash,
taxonomy, watermelon.
Some of the World’s most valuable crops, including watermelon, honey melon, cucumber,
squash, zucchini and pumpkin, belong to the family Cucurbitaceae. We review insights on their
domestication from new phylogenies, archaeology and genomic studies. Ancestral state
estimation on the most complete Cucurbitaceae phylogeny to date suggests that an annual life
cycle may have contributed to domestication. Domestication started c. 11 000 years ago in the
New World and Asia, and apparently more recently in Africa. Some cucurbit crops were
domesticated only once, others multiple times (e.g. melon from different Asian and African
populations). Most wild cucurbit fruits are bitter and nonpalatable to humans, and nonbitterness
of the pulp apparently was a trait favoured early during domestication, with genomic data
showing how bitterness loss was achieved convergently. The genetic pathways underlying
lycopene accumulation, red or orange pulp colour, and fruit size and shape are only just
beginning to be understood. The study of cucurbit domestication in recent years has benefitted
from the increasing integration of archaeological and genomic data with insights from herbarium
collections, the most efficient way to understand species’ natural geographic ranges and climate
adaptations.
I. Introduction
The gradual transition from hunting and gathering to plant
cultivation and animal husbandry began between the end of
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New Phytologist Ó 2019 New Phytologist Trust
the Pleistocene and the beginning of the Holocene, some
12 000–10 000 years ago (Fuller et al., 2014; Arranz-Otaegui
et al., 2018). The resulting sustainable nutrition of large
sedentary populations represents one of the most significant
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2 Review
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Tansley review
transitions in the c. 300 000 year-long history of Homo sapiens
(Larson et al., 2014; Richter et al., 2017). The reasons behind
the implied behavioural changes in various human populations
remain much debated, but are likely to have involved a
combination of climate change, accompanying changes in the
vegetation, prey animal densities, human demography, and
human social systems (Belfer-Cohen & Goring-Morris, 2011;
Larson et al., 2014). Eleven geographic regions have been
identified as centres of plant and animal domestication in the
New World, Africa, the Middle and Near East, Asia and New
Guinea (Piperno, 2011; Fuller et al., 2014; Larson et al., 2014,
and references therein).
Domestication involves humans acting as dispersers and
modifiers of a crop’s biotic and abiotic environment (Larson
et al., 2014). It is a gradual process and often is not restricted
to a single place or human population (reviewed in Meyer
et al., 2012). As a result of this process, crop plants and
domesticated animals share suites of modified traits referred to
as the ‘domestication syndrome’, differentiating them from
their wild ancestors (Darwin, 1868; De Candolle, 1884;
Hammer, 1984; Pickersgill, 2007; Meyer et al., 2012; Stetter
et al., 2017). In plants, the domestication syndrome often
involves larger and more sugary fruits, reduction of physical
and chemical defences in the parts used by humans, a change
towards a more compact architecture, larger seeds, reduction in
seed dormancy, larger inflorescences and non-shattering seeds
(in grasses and legumes).
This review synthesises recent insights with older studies to
produce a big picture of the domestication of Cucurbitaceae
crops, highlighting different domestication trajectories as
informed by phylogenetics, archaeology and genomics. The
gourd family (Cucurbitaceae) has c. 1000 species, including
numerous crops, such as cucumber (Cucumis sativus), bitter
gourd (Momordica charantia), watermelon (Citrullus lanatus),
preserving melon (Citrullus amarus), honey melon (Cucumis
melo), squash and zucchini (Cucurbita pepo), and bottle gourd
(Lagenaria siceraria) (Schaefer & Renner, 2011a,b; Renner &
Schaefer, 2016; Fig. 1). Archaeobotanists have long documented the roles of cucurbits in ancient cultures based on
remains of fruits, seeds and even leaves (e.g. Schweinfurth,
1883, 1884; Piperno, 2000, 2011; Wasylikowa & van der
Veen, 2004), and old texts and illustrations document the
spread of cucurbit crops from India or the Americas to the
Mediterranean and northern Europe (Paris et al., 2012a,b,c,
2013; Paris, 2015). However, it is DNA sequencing of old
and new material (usually leaf tissues), informed by meta-data
from herbarium specimens, that has yielded the most surprising insights. Such work has by now identified closest relatives,
ancestral areas and divergence times of pumpkin, zucchini,
squashes, bottle gourd, bitter gourd, chayote, honey melon,
watermelon, cucumber, bryonies, and sponge gourds (Sanjur
et al., 2002; Erickson et al., 2005; Clarke et al., 2006; Renner
et al., 2007; Volz & Renner, 2009; Schaefer & Renner,
2010b; Sebastian et al., 2010, 2012; Telford et al., 2011a,b;
Filipowicz et al., 2014; Chomicki & Renner, 2015; Endl et al.,
2018).
New Phytologist (2019)
www.newphytologist.com
(a)
(b)
1 cm
10 cm
(c)
(d)
5 cm
15 cm
10 cm
(f)
(e)
1 cm
15 cm
Fig. 1 Cucurbitaceae crops and their wild progenitor to illustrate the
domestication syndrome. (a, b) Honey melon (Cucumis melo). (a) Wild
melon progenitor, Asian agrestis (Cucumis melo subsp. melo f. agrestis).
(b) Domesticated melon (Asian lineage). (c, d) Watermelon (Citrullus
lanatus). (c) Wild watermelon progenitor, Kordofan melon (Citrullus lanatus
subsp. cordophanus). (d) Domesticated watermelon. (e, f) Cucumber
(Cucumis sativus). (e) Wild cucumber progenitor (C. sativus f. hardwickii).
(f) Domesticated cucumber. Photographs credited to: (a) Balkar Singh;
(c) Harry Paris; (b, d, f) Creative commons; (e) Hanno Schaefer.
II. The diversity of cultivated Cucurbitaceae: traits of
major and minor crops
Out of the c. 1000 species of Cucurbitaceae, 10 are of worldwide
economic importance, cultivated globally, and are here considered
‘major crops’ (Table 1); another 23 are of more local commercial
importance, are often cultivated in their native range, and might be
called ‘minor crops’ (Table 2). The distribution of these 33
cultivated species over a phylogeny that samples 554 of the family’s
species and 95 of its 96 genera (Fig. 2) shows that the species used by
humans are fairly clustered. All major crops are cultivated for their
fruit, a particular type of berry called ‘pepo’ that is consumed ripe
(e.g. pumpkin) or unripe (e.g. zucchini), raw (watermelon), cooked
(squash), or pickled (gherkins). Cucurbita pepo is the only major
crop also cultivated for its seeds and the oil pressed from them.
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Table 1. Traits and geographic origins of the major domesticated Cucurbitaceae crops.
Timeline of
domestication
(years BP,
minimum age)
Area of
origin
Area of
domestication
Silverseeded gourd
Mexico
Mexico
W, P
-
Pumpkins, Squashs
South
America
Unknown
Argentina
W, P
4000
Unknown
-
-
Yes (C. argyrosperma
subsp. sororia)
Yes (C. maxima
subsp. andreana)
No
Summer squashs,
zucchini, pumpkins
Mexico
Mexico
A, G, P, W
8000–10 000
No
C. okeechobeensis +
C. lundelliana
Acorn, crookneck
and pattypan
squashes
Texas and
nearby
states
Texas
G, W
-
Yes
C. okeechobeensis +
C. lundelliana
Watermelon
*Red and
black seed melon
(China)
Sudan (?)
Nile Valley
*China (fleshy
seed cultivar)
A, C, P, W?
*C
5000
*400?
Yes, potentially
C. mucosospermus
Mote (1977);
Wasylikowa & van
der Veen (2004);
Chomicki & Renner
(2015); Renner
et al. (2017, 2019)
Wax gourd
Southeast
Asia,
Australasia
Southeast Asia,
Indonesia?
A
2450 or
before
Yes
B. fistulosa
Cucumis melo
subsp. melo
Numerous names for
cultivars of Melon
India and
Australia
Asia
A, G, P
2200
Yes
C. trigonus +
C. picrocarpus
Cucumis sativus
*Cucumber
(Eurasian),
**pickling
cucumber (East
Asian),
***Xishuangbanna
cucumber
Bottle gourd
India
*Asia, **East Asia,
***Xishuangbanna
region
A, C, P, W
***2500
Yes (C. sativus var.
hardwickii)
C. hystrix
Matthews (2003),
Marr et al. (2007),
Kocyan et al.
(2007), Schaefer
et al. (2009)
Walters (1989);
Sebastian et al.
(2010); Endl et al.
(2018)
Renner et al. (2007);
Sebastian et al.
(2010); Qi et al.
(2013)
Africa
A, P
*11 000
**10 000
Yes
L. breviflora
Kistler et al. (2014)
Bitter gourd
Africa
Independently
domesticated in
Eurasia* and
South America**
Africa or India, unclear
C, G
?
Yes
M. angolensis
Schaefer & Renner
(2010a)
Species
New World
Cucurbita
argyrosperma
Cucurbita maxima
Cucurbita
moschata
Cucurbita pepo
subsp. pepo
Cucurbita pepo
subsp. texana
Africa
Citrullus lanatus
Asia and Melanesia
Benincasa hispida
Momordica
charantia
Sister species
References
C. moschata
Sanjur et al. (2002);
Kates et al. (2017)
Sanjur et al. (2002);
Kates et al. (2017)
Sanjur et al. (2002);
Kates et al. (2017)
Smith (1997); Sanjur
et al. (2002); Kates
et al. (2017)
Sanjur et al. (2002);
Kates et al. (2017)
C. ecuadorensis
C. argyrosperma
For the type of evidence for the domestication area; A, archaeological remains; C, other cultural evidence (e.g. linguistic or iconographic); G, genetic diversity of primitive landraces; P, phylogenetic
evidence; W, inferred from wild progenitor distribution. ; (?) uncertainty remaining; ? unknown; *, ** and *** are used when crop species have been independently domesticated.
Review 3
New Phytologist (2019)
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Lagenaria siceraria
Butternut squash
Wild progenitor
found?
Tansley review
Common names
Type of evidence
for area of
domestication
4 Review
Timeline of
cultivation
(years BP,
minimum
age)
Tribe
Common names
Area of origin
Area of cultivation
Evidence for
domestication
Habit
Sexual system
Benincasa fistulosa
Benincaseae
Tinda
NW India (?)
India, Pakistan, E Africa
Yes
Annual
Monoecious
Citrullus amarus
Benincaseae
Preserving melon
South Africa, Namib
desert
Mediterranean
Perennial
Monoecious
>1900
Fruit rind boiled with sugar
for jams
Citrullus colocynthis
Benincaseae
Colocynth
Northern Africa
Perennial
Monoecious
4000
Citrullus
mucosospermus
Benincaseae
Egusi melon
West Africa
Northern Africa, Middle
East to India
West Africa
Documented as crop in
the Mediterranean
region
for > 1900 years
No
No
Annual
Monoecious
Various medicinal uses
from Ancient Egypt on
Oil and protein rich seeds
used for cooking
Coccinia grandis
Benincaseae
Scarlet gourd, Kowai
East Africa
No
Perennial
Dioecious
Cucumis anguria
Benincaseae
Africa, naturalised in the
New World
Yes, nonbitter and
smooth fruit
Perennial
Monoecious
Cucumis melo subsp.
meloides
Cucumis metuliferus
Benincaseae
Cackrey, Maroon
cucumber, West
Indian gherkin
Tibish and Fadasi Melon
India and Southeast
Asia
Tropical regions
Sudan
Monoecious
Kiwano
Annual
Cyclanthera pedata
Sicyoeae
Neotropics
South America
Hodgsonia macrocarpa
Sicyoeae
Stuffing cucumber,
caigua, achocha
Lard fruit
Himalaya
China
Yes, nonbitter and
larger fruit
Yes, larger fruit and
sweeter cultivars
Yes, larger and smooth
fruits
No
Probably annual
Benincaseae
Africa, perhaps Nile
valley
Sub-Saharan Africa
Luffa acutangula
Sicyoeae
Sponge gourd, angled
luffa
Arabian Peninsula,
India
Tropical regions
Luffa aegyptiaca
Sicyoeae
Sponge gourd
Southeast Asia
Melothria mannii (syn.
Cucumeropsis
mannii)
Melothria scabra
Benincaseae
Egusi gourd
Benincaseae
Momordia dioica
Momordiceae
Momordica balsamina
Use
References
Fruit
Schaefer et al. (2009);
Schaefer & Renner
(2011b)
Bailey (1930); Chomicki &
Renner (2015)
Young shoots cooked and
fruits
Fruits pickled
Renner et al. (2017)
Achigan-Dako et al.
(2015); Chomicki &
Renner (2015); Renner
et al. (2017)
Holstein (2015)
Kirkbride (1993)
Endl et al. (2018)
Monoecious
Young fruits eaten cooked,
seeds used in soups
Fruit eaten raw
Perennial
Monoecious
Fruit cooked
Jeffrey (1980)
Perennial
Monoecious
Chien (1963)
Yes, larger fruit
Annual
Monoecious
Tropical regions
Yes, larger fruit
Annual
Monoecious
Central America
West Africa and
Neotropics
No
Perennial
Monoecious
Seeds used to make oil or
eaten roasted
Unripe fruit cooked,
mature dried fruit used as
a sponge
Unripe fruit cooked,
Mature dried fruit used
as a sponge
Seeds
Mexico and Central
America
Mexico and Central
America
No
Perennial
Monoecious
Fruit eaten raw
Schaefer & Renner
(2010b)
South Asia
South Asia, especially
India
Mediterranean?
No
Annual
Dioecious
Leaves as vegetable fruit
boiled
Momordiceae
Mouse melon,
Mexican miniature
watermelon,
pepquinos
Bristly balsa, pear,
spiny gourd
Balsam apple
No
Annual
Monoecious
Momordica
cochinchinensis
Sicana odorifera
Momordiceae
Gac
Southeast Asia
Yes, larger fruit
Perennial
Dioecious
Fruit eaten raw
Cucurbiteae
Cassabanana
Southeast Asia to North
Australia
South America
No
Perennial
Monoecious
Fruit eaten raw
Sicyos edulis (Sechium
edule)
Sicyoeae
Chayote, christophine,
chouchou
Latin America and
Southern United
States
Tropical regions
Schaefer & Renner
(2010a)
Schaefer & Renner
(2010a)
Schaefer & Renner
(2010a)
Schaefer & Renner
(2011b)
Yes, larger fruit, loss of
bitterness and spines
on fruits, increased
sugar content
Perennial
Sicyos (Sechium)
chinantlense
Tropical Africa
Mexico
Worldwide
>500
Fruit eaten as vegetable
Kirkbride (1993)
Filipowicz et al. (2014)
Filipowicz et al. (2014)
Schaefer & Renner
(2010b)
Newstrom (1991);
Sebastian et al. (2012)
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Species
Tansley review
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Table 2. Minor Cucurbitaceae crops.
New
Phytologist
Schaefer & Renner
(2011b)
Schaefer & Renner
(2011b)
Walters (1989)
Schaefer & Renner
(2011b)
Fruit used as a low-calorie
sweetener and in
traditional Chinese
medicine
Seeds used to make oil or
roasted
Seeds used to make oil or
roasted
Fruit cooked
1000–800
Ó 2019 The Authors
New Phytologist Ó 2019 New Phytologist Trust
This include species that are cultivated but not domesticated and species domesticated but only of local importance.
Monoecious
Annual
Yes, larger fruit
China
Sicyoeae
Trichosanthes
cucumerina
Southeast Asia?
Dioecious
Perennial
No
Tropical East Africa
Joliffieae
Telfairia pedata
Tropical East Africa
Dioecious
Perennial
Yes, larger fruit
Tropical West Africa
Fluted gourd, Fluted
pumpkin
Oysternut, Zanzibar oil
vine
Snake gourd, Serpent
gourd
Joliffieae
Telfairia occidentalis
Tropical West Africa
Dioecious
Perennial
No
China
Luo Han Guo
Siraitieae
Siraitia grosvenorii
Southern China and
Northern Thailand
Common names
Tribe
Species
Table 2. (Continued)
Area of origin
Area of cultivation
Evidence for
domestication
Habit
Sexual system
Timeline of
cultivation
(years BP,
minimum
age)
Use
References
Tansley review
Review 5
Minor crops are cultivated for a wide range of purposes including
raw fruits (e.g. Cucumis metuliferus), nutritious seeds (e.g. Citrullus
mucosospermus) or to make oil (e.g. Telfairia occidentalis, T. pedata,
Hodgsonia macrocarpa), cooked fruit (e.g. Trichosanthes
cucumerina), sugary fruit used as a sweetener (Siraitia grosvenorii)
or for their physical (Luffa aegyptiaca used as sponge) or medicinal
properties (Citrullus colocynthis; Barghamdi et al., 2016).
The domestication syndrome of Cucurbitaceae crops includes
nonbitter fruits, increased fruit size, sometimes with higher sugar or
carotenoid content, decreased physical defences (e.g. wild chayote
fruits are spiny), and more compact and less branched growth with
increased apical dominance. Selection of plants with desirable
properties was probably begun by individual farmers and did not
involve mass selection. All crop species went through population
bottlenecks during domestication (Gross & Olsen, 2010). However, the number of rice plants sown by a household would be
significantly higher than that of cucumber or squash plants, and the
population size of founder plants in cucurbit domestication may
therefore have been smaller than in Poaceae crops (Qi et al., 2013).
Traits, such as nonbitter fruits, clearly were consciously selected for
and were not a byproduct of selection for other features (see section
IV.1 ‘Loss of bitterness’).
Most Cucurbitaceae are annual or perennial herbs, and c. 50% of
the species are monoecious, 50% dioecious (Kocyan et al., 2007;
Schaefer & Renner, 2011b). Most major crop species (Table 1) are
annuals with a monoecious sexual system in which every individual
sets fruit. To test whether these traits were present already in the
wild relatives of these crops or are overrepresented among
domesticated forms, we performed a family-wide ancestral state
estimation of life form evolution, scoring species as annual or
perennial based on personal observations, labels of herbarium
specimens and relevant literature. The results reveal that all but one
of the major crop species are nested in lineages with an annual habit,
while minor crops are either annual or perennial (Fig. 2). An annual
life cycle may have facilitated domestication. Cucurbitaceae all have
indeterminate growth, meaning that annual domesticated species
are actually perennials that die at the end of the productive cycle due
to the exhaustion of the vegetative organs imposed by the selection
for high productivity or due to unfavourable climate conditions
outside their centre of origin. In other words, perennial Cucurbitaceae crops are cultivated as annuals, but this is a management
practice, not the result of genetic changes. Perennial wild species
often build up large underground tubers from which annual shoots
emerge (Schaefer & Renner, 2011b) that flower in their first year
(H. Schaefer, pers. obs.).
Most Cucurbitaceae have unisexual flowers, and based on
outgroup comparison, dioecy appears to be the ancestral state in the
family (Zhang et al., 2006). There have been numerous evolutionary changes between monoecy and dioecy (Volz & Renner, 2008;
Schaefer & Renner, 2010b), and the sexual systems of many wild
species are neither reliably known nor can be extrapolated from
herbarium material, especially in climbers in which male and
female flowers appear distant from each other and at different
times. Some cucurbit climbers, such as species of Gurania and
Psiguria, only bear male flowers until they reach sunny conditions
(in the canopy or because of a disturbance) and then form female
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Cogniauxia podolaena
Cogniauxia trilobata
Telfairia pedata
Telfairia batesii
Telfairia occidentalis
mblotii
Ampelosicyos hu
bosseri
Ampelosicyos
s scandens
Ampelosicyo
is
nia central
Austrobryo
antha
onia micr
Austrobry
arensis
onia pilb
Austrobry
gillicola
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m
Austrobr
m elat eriu
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sa
verr uco
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aspera
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Zehneria
perrieri
Zehneria m
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Zehneria em
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Zehneria parv
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Zehneria polycar
pa
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Zehneria maysorensis
Zehneria indica
Zehneria microsperma
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A e r o s ic y o s tr ip il ie
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X e r o s ic y o s ra s
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X e r o a tr i n d u s g ra c ro
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S n o rd a n th u s a n ru m
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a
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A c ti n o le y a m it n g y ta
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H e m s le y a tu rb ro c s c a
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H e m s le y a p a n a v a y i
H e m s le y a e la n s is a
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H e m s le y a c ll ip s n s is
H e m s le y a e m e ie a
H e m s le y a o ig a n th is
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H e m s le y a a m n g e e rm
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G om ls om itr st ep he
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Octo mele
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Tetra meles
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Coriar ia
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Coriari a myrtifo
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Coriaria ruscifoli
Coriaria sarmento sa
Corynocarp us laevigatus
Anisophyllea corneri
Anisophyllea fallax
Combretocarpus rotundatus
Cucumis variabilis
Cucumis althaeoides
Cucumis maderaspatanus
Cucumis afrotropicus
Cucumis leiospermus
Cucumis rumphian
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Cu cum
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C o c c ia lo n ro p e d ii
C c c in ia m a g ic a h y ll
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T ro c h li a n lu ra s re s
T ro c ty n ia c e n ig a
D a s ta n ia e ri a p id s a
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japonica
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tyla
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Zehneria ha
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Z e h n e r i a wallich
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Zehneria samo
donica
Zehneria neocale
Zehneria pisifera
Zehneria guamensis
Zehneria hookeriana
Zehneria keayana
Zehneria mucronata
Tr
ic
ho
T s
T r r ic a n th
ic h
T
T r r ic T r h o o s e s
ic h o ic h s a a n p
ho s
o s n th th e n
T
a
ic
e ta
s
h o r ic h a n n th a n e s s
p
s a o s th e s th e p m o h y
n th a n e s q s a p r r ll a
Tr
u
is
i c T r e s th e la c in q w a u a n ii
ho ic
w
s e
s a h o q u in w a r ib u e fo r a e a
q ll ic r a c li
T T ri n t s a
T ri T ri c h c h h e s n t h u a n h ia te a
c h ri c
os osa t es gu n a
h
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a n n th i c p la a
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T ri n th a n th th e e s s p d a
s
i
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te
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a a
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c h T ri c n th e n th in te e lm e ra
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T
lo e d
T r ri c h th e s n th e p il o b o ia
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os
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T ri s a n n th a b a e le b s is
the es
lu
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L in o s a s b m o n e n s is a
n a n th o r n ta
H a e o s ic e s o e e n n a
Cy
sis
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H
n th a n b u ri a s a m c u ra
e ra u ri a o e
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C y b ra c m e x te d
E ch C yc c la n h y s ic a ii
in o la n th th e ta c n a
pe
e ra ra c h y a
p
E
a u ili a ta
E ch ch in o n p
in o o p e e n in st ra li
pep pon
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E
E ch ch in o n p a b ig e ri s
E ch in op op ep n ic u lo vi i
in op ep on o n w la tu
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M ic
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m go Fr an tz ho id
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E ch
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M ar in oc ys
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M ar ac ro ca ba ta
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Si cy
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Si
cy os
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Si cy
Si cy os ch iri di pt er a
os m
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Si
Si cy cy os hin ns is
os co
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S i c y o Si cy os ed itu s
s ch
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Sic yo
s pa rvi t l e n s e
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Sic yo
Sic yos s gra cili s
die ter
Sic yos
lea e
ma
Sic yos cul atu s
bul bos
us
Sic yos
gal eot
tii
Sic yos
glab er
Sicy os
gua tem
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Sicy os
triqu eter
Sicy os tetra
pter a
Sicy os mon
tanu s
Sicyo s warm
ingii
Sicyo s heller
i
Sicyos villosu
s
Sicyos herbsti
i
Sicyos cucume rinus
Sicyos lanceoloid eus
Sicyos albus
Sicyos hillebrandii
Sicyos debilis
Sicyos maximowiczii
Sicyos waimanaloensis
Sicyos weberbaueri
Sicyos pachycarpus
Sicyos baderoa
Sicyos lasiocephalu s
Sicyos anunu
Sicyos erostrat us
tosus
Sicyos longise
phyllu s
Sicyos macro
us
Sicyo s hispid
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Sicyo s quinq barb atus
Sicy os
thus
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Sicy os
rpus
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Sicy os
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Sicyos
rud era
Sic yos tilo bus
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Sic yos
dav
Sic yos
anu s
me xic lus
yos
Sic
hyl
mic rop life r
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Sic yo an gu lat
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Si cy po lya ca at us
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Si cy cy os lac llin us
Si
os co ol iu s
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Si
al vif ae
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Si cy Si cy os da ra
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Si cy au st ra is
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Si cy ni ns ul lu s
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S ic yo ni ifo ns e
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to
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sp
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H er er m
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pe to sp er m u re ia a ra tr a n ii
E
H er
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B a cy o ia h u rs if o is
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De
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A p ri a n s ic th e s tr o u g e ri
lo s a n e c d im c a
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Me
ra s a a m n d o le im
C e ra to o c a li h y p a x ti c a
m r
m
C e m a rv il le le a a th a te a ta ta
le a c
il
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c r a il la e s
T Ib e rv rv
Ib Ib e m e to e b r ti c o id ll a
e d ia v e is c h y s a
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a
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G r a n r a n ia tu p
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Tr
Momordica suringarii
Momordica macrophylla
Momordica denticulata
Momordica cochinchinens
is
Momordica sphaeroi
dea
Momordica renig
era
Momordica de
nudata
Momordica s
ubangulata
Momordica
laotica
Momordic
a dioica
Mom ordic
a g i l g i a na
Momord
ica ciss
oide
Mom ordi
ca diss ecta s
Mom ordi
ca litto rea
Mom ord
ica car
dios per
Mo mo
rdic a trif
moi des
Mo mo
o l i o l a ta
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Mo mo
a
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Momo
r
Mo mo d i c a e n n e a
phylla
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Mom
o r d i c sp ino sa
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Mom
re
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Mo mo r d i c a c a m y a n a
Mo mo rd ica pa e r o u n e n s
rvi
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M o m rd ica mu fol ia
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M om r d i c a s ltif lor a
i
M om or di ca gl l v a t i c a
ab ra
M om or di ca
pt
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M om or di ca
nu da ar pa
M om or di ca
M om or di ca fri es io ru
M om or di ca tri fo lia m
M om or di ca cl ar ke
M om or di ca an ig os an a
M o or di ca co ry an th a
m
m
M om o r d i c re pe bi fe ra
M om or di a h e n ns
ca
an gu r i q u e
M o or di
ca
st is s i i
M o m o rd
ep
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M o m o rd a cy lli co la al a
ic
mb
M o m o rd a ki
rk ii a la ri a
M o m o rd ic a h
u
M o m o rd ic a b m ili s
M o m o rd ic a se o iv in
ii
M o m o rd ic a b ss ili
M o m o rd ic a a ls a fo li a
M o m o rd ic a in v o lu m in a
M o m o rd ic a w e lw c ra
M o m o rd ic a c h a ra it s c ta
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M o m o rd ic a a n g n ti a ii
ss
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M o m o rd ic a le io ti d a s is
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ic
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S ir a it
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T h a it ia g m e b t u s a m b
ia
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a
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S d o fe v
y u rn b ia ri
S ic y fe v il le nn e e n
S ic y d iu il le a k an s is
P ic y d iu m a ji h a s e n s
P te r d iu m d if fu r o i ia n is
a
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y c r o p o s o n y n a if o
la e p ic y a n th li u
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6 Review
Fig. 2 Phylogenetic distribution of cultivated Cucurbitaceae and ancestral state estimations on a phylogeny sampling 554 of the family’s c. 1000 species of
annual vs perennial taxa. Name of major crop species printed in red (and marked by arrows), names of minor crop species in blue.
flowers (Condon & Gilbert, 1988). In many dioecious species,
prolonged careful observations of numerous individuals also reveal
‘leaky dioecy’, the occasional development of flowers of both sexes
in dioecious individuals (Schaefer & Renner, 2010b).
III. Time and place of domestication
1. The New World as a centre of cucurbit domestication
Several important Cucurbitaceae crop species were domesticated
in the New World in pre-Columbian times (Larson et al., 2014).
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The most prominent are the globally important squashes and
pumpkins (Cucurbita spp.; Table 1; Fig. 3). The genus Cucurbita
had a wide pre-Holocene distribution and was adapted to the
disturbed habitats maintained by large-bodied mammals that
also dispersed the bitter fruits, potentially because these mammals had few bitter taste receptor genes (Kistler et al., 2015).
Population fragmentation inferred from plastid genomes suggests
that the Holocene megafaunal extinction led to a decline in wild
Cucurbita, which were then ‘rescued’ by anthropogenic dispersal
during domestication (Kistler et al., 2015). Archaeological
evidence points to northern South America and Central America
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0.02
100
Review 7
Cucurbita pepo subsp. fraterna Mexico NE
Cucurbita pepo subsp. fraterna Mexico NE
100 Cucurbita pepo subsp. fraterna Mexico NE
Cucurbita pepo subsp. fraterna Mexico NE
Cucurbita pepo subsp. ovifera var. texana US TX
Cucurbita pepo subsp. ovifera var. texana US TX
Cucurbita pepo subsp. ovifera var. texana US TX
Cucurbita pepo subsp. ovifera var. ozarkana US KY
Cucurbita pepo subsp. ovifera var. texana US TX
Cucurbita pepo subsp. ovifera var. texana US MS
Cucurbita pepo subsp. ovifera var. texana US MS
Cucurbita pepo subsp. ovifera var. ozarkana US MO
Cucurbita pepo subsp. ovifera var. ozarkana US MO
Cucurbita pepo subsp. ovifera var. ozarkana US MO
Cucurbita pepo subsp. ovifera var. ozarkana US KY
Cucurbita pepo subsp. ovifera var. ovifera US
Cucurbita pepo subsp. ovifera var. ozarkana US LA
100
Cucurbita pepo subsp. ovifera var. ozarkana US OK
Cucurbita pepo subsp. ovifera var. ozarkana US AK
Cucurbita pepo subsp. ovifera var. ovifera US
Cucurbita
pepo subsp. pepo Guatemala
100
Cucurbita pepo subsp. pepo Mexico NC
Cucurbita pepo subsp. pepo Guatemala
Cucurbita pepo subsp. pepo Mexico SW
Cucurbita pepo subsp. pepo Argentina
Cucurbita
pepo subsp. pepo Argentina
92
Cucurbita pepo subsp. pepo Brazil
Cucurbita lundelliana Belize
Cucurbita lundelliana Honduras
Cucurbita lundelliana Mexico
Cucurbita okeechobeensis subsp. martinezii Mexico
92
Cucurbita okeechobeensis subsp. martinezii Mexico
Cucurbita lundelliana Guatemala
Cucurbita argyrosperma subsp. argyrosperma Mexico SW
Cucurbita argyrosperma subsp. argyrosperma Belize
Cucurbita argyrosperma subsp. argyrosperma Mexico NW
Cucurbita argyrosperma subsp. sororia Mexico W
Cucurbita argyrosperma subsp. sororia Mexico SW
92
Cucurbita argyrosperma subsp. argyrosperma Nicaragua
Cucurbita argyrosperma subsp. argyrosperma US AZ
Cucurbita argyrosperma subsp. argyrosperma var. palmeri Mexico NW
Cucurbita argyrosperma subsp. sororia Mexico NW
Cucurbita argyrosperma subsp. sororia Mexico SW
Cucurbita argyrosperma subsp. sororia Mexico E
Cucurbita argyrosperma subsp. argyrosperma var. stenosperma Mexico NW
100 Cucurbita argyrosperma subsp. sororia Mexico W
Cucurbita argyrosperma subsp. sororia Mexico E
Cucurbita argyrosperma subsp. argyrosperma Guatemala
Cucurbita moschata Guatemala
Cucurbita moschata Mexico SE
Cucurbita moschata Brazil
100
Cucurbita moschata Guatemala
Cucurbita moschata Brazil
Cucurbita moschata Mexico NW
100
Cucurbita moschata Bolivia
Cucurbita moschata Puerto Rico
100
Cucurbita moschata US IA
Cucurbita maxima subsp. maxima Bolivia
Cucurbita maxima subsp. maxima Bolivia
Cucurbita maxima subsp. maxima Brazil
Cucurbita maxima subsp. maxima Peru
Cucurbita maxima subsp. maxima Mexico SW
Cucurbita maxima subsp. andreana Argentina
Cucurbita maxima subsp. maxima Argentina
100
Cucurbita maxima subsp. maxima Bolivia
Cucurbita maxima subsp. maxima Argentina
Cucurbita maxima subsp. maxima Argentina
100
Cucurbita maxima subsp. maxima US MN
Cucurbita maxima subsp. andreana Argentina
Cucurbita maxima subsp. andreana Argentina
93
Cucurbita maxima subsp. andreana Argentina
Cucurbita ecuadorensis Ecuador
93
Cucurbita ecuadorensis Ecuador
Cucurbita pepo subsp. ovifera var. texana US MS
72
Cucurbita ficifolia US
Cucurbita ficifolia Mexico SW
Cucurbita foetidissima Mexico Zacatecas
Cucurbita foetidissima US TX
Cucurbita foetidissima Mexico NC
Cucurbita foetidissima Mexico NC
Cucurbita foetidissima Mexico SW
Cucurbita pedatifolia Mexico
Cucurbita foetidissima US NM
Cucurbita palmata US CA
100
Cucurbita pedatifolia Mexico
Cucurbita pedatifolia Mexico
Cucurbita digitata Mexico
Cucurbita cordata Mexico
100
Cucurbita digitata US AZ
Cucurbita sp.
Cucurbita cordata Mexico
Cucumis
Outgroups
Citrullus
Fig. 3 Phylogeny and domestication of Cucurbita. The maximum likelihood (ML) tree was inferred from 44 nuclear loci taken from Kates et al. (2017). Bluecoloured taxa indicate likely progenitor taxa, red-coloured taxa indicate domesticated species. ML bootstrap support values are shown for the backbone and the
main clades (all values are shown in Kates et al., 2017).
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as places of the earliest pumpkin domestication, c. 10 000 years
ago (Smith, 1997).
Of the four major crop species in the genus Cucurbita, C. pepo is
native to North America (Northeast Mexico, and the Southeast and
Central United States; Bailey, 1943; Paris et al., 2012c), and
archaeological remains suggest an initial domestication some
8000–10 000 yr ago in Mexico (Smith, 1997). Independent domestication occurred in Eastern North America (Sanjur et al., 2002).
These two domestication events led to the forms now classified as
C. pepo subsp. pepo and C. pepo subsp. ovifera (Paris et al., 2012c;
Table 1; Fig. 3). No wild populations of subsp. pepo have been found,
but wild populations of subsp. ovifera occur in Texas and nearby
states, and a 3rd taxon (C. pepo subsp. fraterna) occurs in Northeast
Mexico (Nee, 1990). However, C. pepo subsp. ovifera is not monophyletic, instead appearing in at least two places in a nuclear
phylogeny, with a mix of domesticated and nondomesticated forms,
suggesting either introgression, multiple domestication centres and/
or broad domestication bottlenecks (incomplete lineage sorting in the
crop) (Kates et al., 2017; our Fig. 3). American cultivars of C. pepo
subsp. pepo reached Italy in the 16th century, where in the mid-19th
century they gave rise to the cultivar group known as zucchini. From
Italy, zucchini returned to the Americas, and today, they are one of the
most widely cultivated crops of the family (Lust & Paris, 2016).
The second domesticated species of Cucurbita is C. maxima, with
the subspecies maxima (Hubbard squash, buttercup squash, giant
pumpkin) and andreana. The former was cultivated as early as 4000
BP along the coast of Peru where it may have been domesticated, but
apparently never left the Neotropics during pre-Columbian times
(Sauer, 1993; Piperno & Stothert, 2003). The other subspecies,
andreana, appears to have been domesticated in what is today
Argentina (Nee, 1990; Sanjur et al., 2002; Kates et al., 2017).
The third domesticated species of Cucurbita, C. moschata – the
butternut squash – may have originated in Northern South
America (Sanjur et al., 2002), consistent with high landrace
diversity, and commonness of landraces with primitive traits such
as small dark seeds, lignified, warty rind and bitter pulp (Nee,
1990). However, nuclear sequence data cast doubt on a South
American origin of this species (Kates et al., 2017).
The fourth domesticated species of Cucurbita, C. argyrosperma is
native to Mexico (Sanjur et al., 2002; Kates et al., 2017) and probably
was domesticated there, although the timeline of its domestication
remains unclear because of a lack of archaeological remains.
Another Cucurbitaceae crop from a different genus domesticated in the New World is Sicyos edulis, the chayote. Linguistic data,
together with cultivar genetic diversity, pinpoint Mexico as its
centre of domestication (Newstrom, 1991), consistent with a
biogeographic analysis showing Mexico as the ancestral area of the
clade containing chayote (Sebastian et al., 2012). Hernandez
(1550) documented the use of the chayote by the Aztecs. It became
a worldwide crop in tropical, subtropical and warm temperate
regions in the 19th century when it was introduced in Africa,
Southern Europe, Asia and the West Indies, with the precise dates
of introduction known in most cases (Newstrom, 1991). A
potential wild progenitor population of chayote has been found in
Mexico, with small, spiny and bitter fruits, but some less bitter and
containing sugar (Newstrom, 1991).
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Melothria mannii is a minor crop (Table 2) cultivated for its
nutritious seeds as a so-called ‘egusi-crop’ (for making stews) in
both West Africa and Central and South America. Biogeographic
reconstruction indicates that it is native to America (Schaefer &
Renner, 2010a; treating the species under the erroneous name
Melothria sphaerocarpa). Whether it has been domesticated independently in America and Africa is unclear. It could have been
brought to Africa as a domesticate during the slave trade, but
natural transatlantic dispersal of either wild or cultivated forms
cannot be excluded (Schaefer & Renner, 2010a).
2. Africa as a centre of cucurbit domestication
The genus Citrullus is the most economically important Cucurbitaceae lineage in Africa where it has seven species (Chomicki &
Renner, 2015) of which several are cultivated and some are used as
bush food (C. amarus, C. naudinianus). The taxonomy of the genus
Citrullus until recently contained misapplications of names,
including that of the watermelon, C. lanatus, itself (Renner et al.,
2014; Chomicki & Renner, 2015). The erroneous nomenclature
led to a number of confusions, including the reference to ‘wild’,
‘semi-wild’ and ‘domesticated’ populations of watermelon that are
in fact distinct species ‘separated’ by undoubted wild species.
Citrullus lanatus is the most economically important species in the
genus. It was long thought to originate from South Africa because
of a taxonomic mistake involving the oldest collection of a wild
South African species described by a student of Linnaeus, which in
the 1930s was wrongly synonymised with the cultivated watermelon (Bailey, 1930). Phylogenetic evidence, including DNA from
the original specimen collected near Cape Town in 1773 by
Linnaeus’s student Carl Peter Thunberg, showed that no South
African material is closely related to the domesticated watermelon.
The earliest archaeological evidence of cultivated watermelon
consists of seeds dated to c. 5000 BP (8000? BP) from Wan
Muhuggiag in Libya (Wasylikowa & van der Veen, 2004). An
oblong, large fruit served on a tray and with the characteristic
striped fruit skin of watermelon is shown on a wall painting in a
Pharaonic tomb from Meir, Northwest of Asyut (reproduced in
Paris, 2015), suggesting that the fruit was eaten raw, which would
indicate the availability of sweet, nonbitter watermelons in Egypt
4000 years ago (Chomicki & Renner, 2015).
Four hypotheses have been proposed for the origin of the
watermelon: First, that it descends from the northern African
colocynth (C. colocynthis; Singh, 1978; Sain et al., 2002;
McCreight et al., 2013). Second, that it derives from the South
African citron melon, C. amarus (Robinson & Decker-Walters,
1997; Maynard & Maynard, 2000; Rubatsky, 2001). Third, that it
stems from the West African C. mucosospermus (Guo et al., 2013;
Chomicki & Renner, 2015), and fourth, that it both originated
from and was domesticated in Northeastern Africa (Paris, 2015). A
phylogenetic analysis of Citrullus (Chomicki & Renner, 2015),
together with genetic, archaeological and historical data (reviewed
by Paris, 2015) rejects the first two hypotheses, leaving West Africa
and Northeast Africa. Phylogenomic analyses of nuclear gene
sequences suggested that the white-fleshed Sudanese Kordophan
melon is the closest relative of the domesticated watermelon
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Review 9
Fig. 4 The phylogeny and domestication of
Citrullus. The phylogeny results from a
maximum likelihood (ML) analysis of 143
nuclear loci from Renner et al. (2019) with ML
bootstrap values shown at branches. ML
analysis of a matrix with 100 plastid loci
yielded the same topology, with high
bootstrap support at all nodes. Blue-coloured
taxa indicate likely progenitor, red-coloured
taxa indicate domesticated species.
(Renner et al., 2019; Fig. 4). The lack of bitterness and high sugar
content of Kordophan melons (Ter-Avanesyn, 1966), however,
leaves open the possibility that these melons represent a landrace.
Phylogenomic data also imply that the West African egusi melon,
C. mucosospermus, bred for its nutritious seeds (Achigan-Dako
et al., 2015), was domesticated from a different gene pool than that
of the watermelon.
Another crop in the genus Citrullus is the preserving melon,
C. amarus, which originates from Southern Africa (Chomicki &
Renner, 2015; Renner et al., 2017 provide a distribution map).
This species, referred to as ‘citron melon’ in its wild South African
form, is an important crop in the Mediterranean region where the
ripe fruit, including its rind, is boiled with sugar to make jams
(Laghetti & Hammer, 2007). It is also used in specialty baking, for
example, in fruit cake mixes and Christmas baking in Mexico and
the United States (Bush, 1978). The species was introduced into
the Mediterranean region from at least the Roman era, as evidenced
by mention in a Latin cookbook (De Re Coquinaria, AD 77–516) as
citrium (Paris, 2015), and there is archaeological and iconographic
evidence that it was a widely used crop all around the Mediterranean and Europe from at least the 14th century (Paris et al., 2013;
Paris, 2015). The species was also introduced to Australia by
Afghan cameleers in the mid 1800s to early 1900s, who used its
fruits as a feed source for their camels; it is now a weed of summer
fallows in Australia (Shaik et al., 2017).
The colocynth, C. colocynthis, has also been cultivated since
Ancient Egyptian times as a medicinal plant and a source of oil but
has not been domesticated. Colocynth seeds are found from 5000
BP (8000 BP) onwards in archaeological sites in Libya, Egypt and the
Near East (Wasylikowa & van der Veen, 2004), and the species may
have reached India and Pakistan by human transport.
3. Asia and Melanesia as centres of cucurbit domestication
The most important Cucurbitaceae crop from Asia is the
cucumber, Cucumis sativus. Cucumbers have been domesticated
from wild Indian C. sativus var. hardwickii (Qi et al., 2013), which
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New Phytologist Ó 2019 New Phytologist Trust
has small bitter-tasting or sour fruits that are ellipsoid or subglobose
and 5–8 cm long (Fig. 1e); it is known from India and Northwest
and West Thailand, growing wild and sold in local markets. Three
main cultivar groups of cucumber were subsequently selected for
distinct purposes, namely Eurasian cucumbers (our slicing cucumbers eaten raw and immature), East Asian cucumbers (pickling
cucumbers) and Xishuangbanna cucumbers (Fig. 5, inset). Based
on demographic modelling, the East Asian C. sativus cultivars
diverged from the Indian cultivars c. 2500 years ago, that is close to
a Chinese text reporting the introduction of cucumber to China
during the Han dynasty (Qi et al., 2013). The Xishuangbanna
cultivar (C. sativus var. xishuangbannanensis) was selected for high
b-carotene content in the mature pulp; its fruits are eaten boiled or
raw during different stages of maturity (Yang et al., 1991; Renner,
2017).
Honey melon (Cucumis melo) was domesticated at least once in
Asia and once in Africa (Endl et al., 2018; Fig. 5). The oldest melon
remains from Asia date to 3000 BC in China (Watson, 1969) and to
2300–1600 BC in the Indus valley (Vishnu-Mittre, 1974). The oldest
African melon seeds date to a site from 3700 to 3500 BC in Lower
Egypt (van Zeist & de Roller, 1993; El Hadidi et al., 1996). The
honey melon cultivars grown today can be traced back to two wild
lineages that are estimated to have diverged 1–3 Ma. The first one is
restricted to Asia (C. melo subsp. melo), while the second, C. melo
subsp. meloides Endl & H. Schaef., is widespread throughout Africa.
The Asian lineage gave rise to all modern cultivars including the
commercially important ‘Galia’, ‘Cantaloupe’, and ‘Yellow Honeydew’ melons, while the African lineage gave rise to the ‘Tibish’ and
‘Fadasi’ melons, landraces still grown in the Sudanese region but
gradually being replaced by imported cultivars from Asia. A third
wild C. melo lineage is restricted to Australia and New Guinea but
apparently was never domesticated (Endl et al., 2018). The C. melo
clade is sister to a long overlooked Indian perennial, C. trigonus and
the Australian C. picrocarpus (Endl et al., 2018).
Lagenaria siceraria, the bottle gourd, the dry empty fruits of
which are used as watertight containers, is native to Africa
(Table 1). The species appears to have been cultivated as early as
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C. melo ssp. melo f. agrestis ("C. melo var. texanus") Dale Thomas 86774 USA (Louisiana)
C. melo ssp. melo f. agrestis ("C. callosus") Eig & Zoharys.n. Israel
C. melo ssp. melo f. agrestis Mitchell & Schaefer 53 Madagascar
C. melo ssp. melo f. agrestis ("C. callosus") unknown coll. (USDA PI435284) Iraq (Damirdagh)
C. melo ssp. melo f. agrestis ("C. callosus") Schaefer 2017/29 India
C. melo ssp. melo f. agrestis unknown coll. (USDA PI386046) Iran
C. hystrix
C. melo ssp. melo f. agrestis Aye Htwe 020699 Myanmar
C. melo ssp. melo f. melo cv. "Tirama" Ouedraogo s.n. Burkina Faso
C. melo ssp. melo f. agrestis (C. pubescens) Achigan-Dako Cuc48 India
C. melo ssp. melo f. agrestis Eigs.n. Afghanistan
C. sativus var. hardwickii
C. melo ssp. melo f. melo cv. "Moussa"Achigan-Dako 1006SE033B Mali
C. melo ssp. melo f. melo cv. "Conomon" Schaefer s.n. Cambodia
C. melo ssp. melo f. melo cv. "Ginsen Makuwa" Hayase s.n. (USDA PI420176) Japan
C. melo ssp. melo f. melo cv. "Tendral" Fantaccione et al. s.n. Mediterranean
C. melo ssp. melo f. melo cv. "Madras" Fantaccione et al. s.n.I taly
Xishuangbanna cucumber
C. melo ssp. melo f. melo cv. "Songwhan Charmi" unknown coll. (USDA PI161375) South Korea
C. melo ssp. melo f. melo cv. "Plum Granny” Schaefer 2017/32 Mediterranean
69 C. melo ssp. melo f. melo cv. "Ao Oo Naga Shima Uri" Schaefer 2017/33 Japan
C. melo ssp. melo f. melo cv. "Kedai Shirouri" Schaefer 2017/191 Japan
C. melo ssp. melo f. melo cv. "Tigger" Schaefer 2017/35 Turkey
C. melo ssp. melo f. melo cv. "KYpickles" Schaefer 2017/27 Taiwan
C. melo ssp. melo f. melo cv. "Melon Voat ango" Schaefer 2017/37 Madagascar
C. melo ssp. melo f. melo cv. "Snap Melon" Schaefer 2017/34 India
C. melo ssp. melo f. agrestis Koppar et al. KSM531 (USDA PI614521) India
Eurasian cucumber
C. melo ssp. melo f. agrestis Mehra1819 (USDA PI536478) Maldives
C. melo ssp. melo f. agrestis Mehra1733 (USDA PI536473) Maldives
C. melo ssp. melo f. agrestis Feare & Van de Crommenacker 2 Seychelles
C. melo ssp. melo f. melo cv. "Freeman’s cucumber" unknown coll. (C136 COMAV UPV) Japan
C. melo ssp. melo f. melo cv. "Conomon" Schaefer 2010/20 Cambodia
C. melo ssp. melo f. melo unknown cv. Attere & Mlongoti ZM/A 5317 (USDA PI505599) Zambia
C. melo ssp. melo f. melo cv. "Queen Anne’s pocketmelon" unknown coll. (USDA PI273438) Switzerland
C. melo ssp. melo f. melo cv. "Chinensis Nabunkin" unknown coll. (C158 Melrip) China
C. melo ssp. melo f. melo cv. "Kakru" Koelz 8786 (USDA PI164493) India (Rajasthan)
C. melo ssp. melo f. agrestis Sahare & Srinivasu s.n. India (Maharashtra)
East Asian cucumber
97 C. melo ssp. melo f. agrestis Mitchell & Schaefer 67 Madagascar
1 C. melo ssp. melo f. agrestis Mitchell & Schaefer 68 Madagascar
C. melo ssp. melo f. agrestis Feare & Van de Crommenacker 1 Seychelles
C. melo ssp. melo f. agrestis ("C. dudaim") Podlech 12605 Afghanistan
C. melo ssp. melo f.melo unknown cv.Gossweiler 10474 Angola
C. melo ssp. melo f. agrestis Sulit 5259 Philippines (Luzon)
C. melo ssp. melo f. agrestis ("C. callosus") unknown coll. (C128 COMAV UVP) India
C. melo ssp. melo f. agrestis ("C. dudaim") Podlech 32603 Afghanistan
C. melo ssp. melo f. agrestis Ali & Pandey 1019 India (Bihar)
C. melo ssp. melo f. agrestis ("C. trigonus") unknown coll. (USDA Ames 24297) Pakistan
C. melo ssp. melo f. melo cv. "Vellari" Koelz 8956 (USDA PI164320) India
C. melo ssp. melo f. melo cv. "Melon Quito" Schaefer 2017/44 Mediterranean
C. melo ssp. melo f. melo cv. "Vert Grimpant" Schaefer 2017/36 France
66 C. melo ssp. melo f. melo cv. "Piel de Sapo" Schaefer 2017/30 Mediterranean
C. melo ssp. melo f. melo cv. "Galia"Schaefer 2017/192 Spain
C. melo ssp. melo f. melo cv. "Yellow Honeydew" Schaefer 2017/193 Spain
99
C. melo ssp. melo f. melo cv. "Cantaloupe" Schaefer 2017/197 Spain
1
C. melo ssp. melo f. melo cv. "Chate Carosello" unknown coll. (C122 Melrip) Italy
C. melo ssp. melo f. melo cv. "Delice de latable" Schaefer 2017/43 Mediterranean
C. melo ssp. melo f. melo cv. "Moussa" Achigan-Dako71ku77 Niger
C. melo ssp. melo f. melo cv. "Petit Grisde Rennes" Schaefer 2017/45 Mediterranean
C. melo ssp. melo f. melo cv. "Armenische Gurke" Schaefer 2017/31 Turkey
C. melo ssp. melo f. melo cv."Ananas à chair verte" Schaefer 2017/190 Mediterranean
C. melo ssp. melo f. melo cv."Prescott à fond blanc" Schaefer 2017/46 Mediterranean
C. melo ssp. melo f. melo cv. "Flexuosus Faqous Sahouri" Arafeh & Altarada s.n. Palestine
C. melo ssp. melo f. agrestis (C. jucundus) Telford 13313 Australia (Queensland)
C. melo ssp. melo f. agrestis (C. jucundus) Telford 13384 Australia (Queensland)
85
C. melo ssp. melo f. agrestis (C. jucundus) Telford 11472 Australia (Queensland)
0.99
C. melo ssp. melo f. agrestis (C. jucundus) Craven & Schodde 884 New Guinea
C. melo ssp. melo f. agrestis (C. jucundus) Van Leeuwin TCMBC14NE Australia (Pilbara)
C. melo ssp. meloides Achigan-Dako 103laa Togo
C. melo ssp. meloides Bartha s.n. Nigeria
C. melo ssp. meloides Achigan-Dako 06NIA061 Ghana
68 C. melo ssp. meloides Baldwin 15591 (USDA PI185111) Ghana
C. melo ssp. meloides unknown coll. (CUM287 C38 COMAV UPV) Nigeria
100
82 C.melo ssp. meloides Achigan-Dako 07NIA1003 Benin
1
C. melo ssp. meloides Achigan-Dako 967Kuo83 Niger
96 96 C. melo ssp. meloides Schaefer s.n. Cabo Verde (Sal)
90 1 1 C. melo ssp. meloides Schaefer 2016/250 Cabo Verde (Boavista)
C. melo ssp. meloides cv."Tibish" unknown coll. (Melrip) Sudan
C. melo ssp. meloides ("C. ambigua") Kotschy 352 Sudan
97
C. trigonus Pandey12513 India
1
C. trigonus Naudins.n. India (cult. Paris Bot. Garden)
100
100 C. picrocarpus Copeland 4515 Australia (New South Wales)
1 100 1 C. picrocarpus Telford 13397 Australia (New South Wales)
100 C. picrocarpus Mitchell 3076 Australia (Northern Territory)
1
C. picrocarpus Telford 13389 Australia (Northern Territory)
1
100
C. rumphianus ssp. tomentosus De Wilde & Duyfjes 21757 Indonesia (Sulawesi)
95
100
1
C. rumphianus ssp. rumphianus Wieringa 1872 Indonesia (Sulawesi)
70
1
C. argenteus Barnsley1656 Australia (Queensland)
1
C. leiospermus Wight1112b India
93
69
C. variabilis Wilson 8389 WesternAustralia
100
64 0.99
C. maderaspatanus Siddarthan s.n. India (Tamil Nadu)
1
C. althaeoides Brennan 2576 Australia (NorthernTerritory)
98
C. ritchiei Filipowicz et al.10India (Kerala)
1
85
C. gracilis Phonsena et al. 5651 Thailand
73
C. silentvalleyi Filipowicz et al. 29 & Sinclair 3589 India (Kerala)
70
96
C. setosus Ritchie 321 India (Kerala)
98
0.99
C. indicus Ritchie 67 India (Kerala)
1
99
C. debilis Petelot 2193 Vietnam
1
100
C. sativus var. hardwickii Phonsena et al. 5654 Thailand
100
1 C. sativus var. sativus Renner 2822 China
99
1
C. hystrix Suddee et al. 2503 Thailand
1
85
C. costatus Forster 9514 Australia (Queensland)
100
1
C. queenslandicus Telford 13316 Australia(Queensland)
1
C. umbellatus Sebastian 15 Australia (Northern Territory)
99
C. dinteri unknown coll. (UPV13365) South Africa
100
1
C. sagittatus Decker-Walters 1124 Namibia
1
C. globosus Erbens.n. South Africa (Namaqualand)
86
C. prophetarum Rechinger28768 Pakistan
68 1
C. pustulatus (USDA PI343699) Nigeria
93
C. insignis Schaefer 2017/196 East Africa
78
C. zambianus Attere & Mlongoti (USDA PI505608) Zambia
61 0.99
C. dipsaceus Schaefer 05/200 Tanzania
C. anguria Mitchell & Schaefer 65 Madagascar
100
C. figarei Achigan-Dako 61ku231 Burkina Faso
1
C. messorius Bally B15187 Kenya
81 C. africanus Schaefer 2017/26 South Africa
76
C. quintanilhae Beitbridge s.n. Botswana
C. myriocarpus Renner et al. 2801 South Africa
C. kalahariensis Maggis 1036 Namibia
88
C. heptadactylus Giess 168 & UPV13367 South Africa
1
C. zeyheri Decker-Walters 1114 South Africa
91
C. aculeatus Schaefer 2017/194 East Africa
1
C. ficifolius Achigan-Dako Cuc67 & Weiss s.n. East Africa
88
C. baladensis Thulin et al. 7464 Somalia
80 0.99
C. rigidus Schaefer 2017/39 Africa
C.
meeusei Schaefer 2017/28 South Africa
94
C.
thulinianus
Yohaness
3611 Somalia
0.99
C. carolinus Schaefer 2017/195 Africa
95
C. pubituberculatus Thulin 6321 Somalia
0.99
C. canoxyi Thulin et al. 9864 Yemen
96
C. hastatus Kuchar 17327 Somalia
1
C. sacleuxii Schaefer05/411 Tanzania
98
C. rostratus Babuker 8712 Nigeria
1
C. metuliferus De Winter & Marais 4614 Angola
C. bryoniifolius Wilkins 214b South Africa
69
C. clavipetiolatus Merxmueller 960 Namibia
95
C. asper Giess et al. 6238 & Volk 2789 Namibia
1
C. subsericeus Schaefer 05/450 Tanzania
100
C. kelleri Thulin et al. 10578 Somalia
1
C. cinereus Giess15436 & Maggis et al. 633 Namibia
100
C. humifructus Merxmueller & Giess 30150 Namibia
1
C. hirsutus De Saeger 1323 & Zimba et al. 874 Zambia
Muellerargia timorensis Telford & Sebastian 13307 Australia (Queensland)
Muellerargia jeffreyana Cours 5586 Madagascar
0.007
Melon
Cucumber
97
1
100
1
100
1
Fig. 5 The phylogeny and domestication of Cucumis. The maximum likelihood (ML) tree was inferred from six plastid and one nuclear locus from Endl et al.
(2018), with ML support above branches and Bayesian poster probabilities below branches. Blue-coloured taxa indicate likely progenitor taxa, red-coloured
taxa indicate domesticated taxa. The inset shows the three domestication directions of the cucumber, C. sativus, based on Qi et al. (2013). Photograph credited
to: bottom right inset: Michel Pitrat.
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11 000 years ago in Asia and independently in the Americas, where
it was widespread 8000 BP (Erickson et al., 2005; Kistler et al.,
2014). For Polynesia, genetic data suggest arrivals from both Asia
and South America, after the species had become a well established
crop in those regions (Clarke et al., 2006). An older scenario
suggested that the bottle gourd was brought to the New World by
Paleoindians as they colonised the continent (Erickson et al.,
2005), but this would imply that a tropical plant could have been
planted and harvested under Arctic climate conditions. A more
recent phylogenetic analysis of a denser sample of archaeological
wild and cultivated American and Asian bottle gourds indicated
that the species was brought from Africa to Eurasia by humans, but
reached America by natural transoceanic dispersal from Africa
before the arrival of humans there (Kistler et al., 2014). Strangely,
archaeological evidence for early bottle gourd cultivation is
restricted to the Pacific coast of South America, which does not
match the species’ presumed transoceanic arrival from Africa.
Bottle gourd used to be an important vegetable in Europe, later
replaced by zucchini (Lust & Paris, 2016).
The bitter gourd, Momordica charantia, another major cucurbit
crop (Table 1), is native to Africa (Schaefer & Renner, 2010b) and
Madagascar, but today is most extensively used in Asian cuisines. Its
use in Kerala (Southern India) is documented from the 17th century
onwards (Rheede, 1688; Marr et al., 2004). It remains unclear
where this important crop was domesticated, and more sampling of
landraces and wild forms from Madagascar, mainland Africa and
Southern India is necessary to confirm its region of domestication.
The wax gourd, Benincasa hispida, is documented from an
archaeological site in Thailand dated from 9980 to 9530 BP
(Pyramarn, 1989), and in New Guinea, rind and seeds have been
found at the Kuk swamp archaeological site (Golson et al., 2017)
dated to 2450 BP (Matthews, 2003). Seed size does not resolve the
status of these archaeological finds as cultivated or wild because at
least the size of the New Guinean seeds is within the range of
domesticates (Marr et al., 2007). The related minor crop Tinda or
Indian round gourd, Benincasa fistulosa (syn. Praecitrullus
fistulosus), is cultivated in India and Pakistan and at a very small
scale in East Africa, where it has been introduced. Its origin and area
of domestication are unclear but wild forms exist in Northwest
India (Renner & Pandey, 2013).
The area of domestication of the sponge gourd, Luffa aegyptiaca,
which occurs throughout Southeast Asia, is unknown and the entire
genus with eight species worldwide is surprisingly poorly understood (Marr et al., 2005; Filipowicz et al., 2014). Small-fruited wild
forms occur in Australia and Indonesia (Marr et al., 2005). Wild
forms of the angled loofah, L. acutangula, are known from the Arab
Peninsula and India (Filipowicz et al., 2014). Interestingly, none of
the three Neotropical Luffa species has been domesticated.
IV. The genomics of Cucurbitaceae domestication
So far, 11 reference genomes of cucurbits have been produced,
namely C. sativus var. sativus cv 9930 and cv Gy14, one wild
cucumber (C. sativus var. hardwickii PI 183967), one cultivated
melon (C. melo cv DHL92), two cultivated watermelons (C. lanatus subsp. vulgaris cv 97103 and cv Charleston Gray), four
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Review 11
cultivated Cucurbita species (C. maxima cv Rimu, C. moschata cv
Rifu, C. pepo cv MU-CU-16, and C. argyrosperma), and one
cultivated bottle gourd (Lagenaria siceraria cv USVL1VR-Ls)
(Huang et al., 2009b; Garcia-Mas et al., 2012; Guo et al., 2013; Qi
et al., 2013; Sun et al., 2017; Wu et al., 2017; Wang et al., 2018;
Montero-Pau et al., 2018; Ruggieri et al., 2018; Barrera-Redondo
et al., 2019), and the number is rapidly increasing. Zheng et al.
(2019) summarised the genomic resources available by 2018.
Comparisons of nondomesticated wild forms with domesticated
accessions imply that domestication of cucurbit fruits always first
required loss of fruit bitterness, a trait conferred by toxic
cucurbitacins (Zhou et al., 2016). Selection also affected the seed
coat, carotenoid content and sugar content. Below we summarise
how this may have occurred. We restrict our review of comparative
and functional genomics of cucurbit crop traits to traits directly
relevant to domestication. Molecular mechanisms underlying
flower sex-determination, fruit development, and spine development in cucumber are reviewed by Che & Zhang (2019).
1. Loss of bitterness
Some wild cucurbit species have sweet fruit pulp, and some of these
are minor crops (Cucumis anguria, Cucumis metuliferus, Melothria
scabra); others are bush food collected from the wild and eaten by
kids, such as the fruit pulp of wild Kedrostis foetidissima, Momordica
species, Solena heterophylla, and some Trichosanthes (e.g. Murthy
et al., 2013). Most wild cucurbits, however, have bitter fruits, with
bitterness conferred by a group of terpenoid compounds called
cucurbitacins. Cucurbitacins are very effective in direct plant
defence against herbivores and are present in leaves, roots and fruits
in many nondomesticated cucurbits. With the exception of the
bitter gourd (Momordica charantia), for which some cultivars are
very bitter when it is harvested, Cucurbitaceae fruit crops have lost
bitterness during domestication. Nonbitter remains of the squash
Cucurbita moschata that date to 9200 BP indicated that automatic
selection (sensu Harlan et al., 1973) for nonbitter fruits occurred
very early (Piperno & Dillehay, 2008).
The Bi gene confers bitterness to the whole plant (Huang et al.,
2009 and references therein), and a genetic and biochemical study
showed that Bi encodes a cucurbitadienol synthase that catalyses the
first committed step in cucurbitacin C biosynthesis in cucumber
(Shang et al., 2014). Two bHLH transcription factors regulate
cucurbitacin C biosynthesis by upregulating Bi in the leaves (Bl )
and fruits (Bt) directly via binding in the E-box elements of the Bi
promoter (Shang et al., 2014). In cucumber, no selective sweep was
associated with the Bi gene (Qi et al., 2013), suggesting that loss of
cucurbitacin biosynthesis in the whole plant would have been
deleterious, even in cultivated crops (notably in terms of defence
against generalist herbivores). Examination of different cucumber
lines with varying bitterness has revealed that domestication of
nonbitter cucumber occurred via the downregulation of Bt, either
by mutation in its cis-acting elements or by affecting the binding site
(Qi et al., 2013; Shang et al., 2014; Zhou et al., 2016). A genomic
analysis of homologues comparing cucumber, melon and watermelon (producing cucurbitacin C, B and E, respectively) revealed a
convergent domestication sweep at the Bt loci and the loss of
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Tansley review
bitterness is, in all cases, due to convergent mutations at this locus
(Shang et al., 2014; Zhou et al., 2016). Selected mutations in an
upstream regulatory gene controlling the expression of a given
pathway in specific tissue may be common during domestication, as
this can help avoid pleiotropic effects associated with modification
of the pathway itself (Lenser & Theißen, 2013).
2. Selection for sweetness
For several Cucurbitaceae crop species, especially watermelon
(Citrullus lanatus) and honey melon (Cucumis melo), selection for
sweet fruits has occurred during domestication. Genome analysis
and transcriptomics in the watermelon revealed that a-galactosidase, insoluble acid invertase, neutral invertase, sucrose phosphate
synthase, UDP-glucose 4-epimerase, soluble acid invertase and
UDP-galactose/glucose pyrophosphorylase are the main enzymes
that regulate sugar unloading and metabolism during ripening
(Guo et al., 2013). In total, 62 sugar metabolism genes and 76 sugar
transporter genes have been annotated, with 13 and 14, respectively, differentially expressed in fruit flesh (Guo et al., 2013). In
honey melon, 63 genes involved in sugar metabolism have been
annotated (Garcia-Mas et al., 2012). Of the sugar transporters
found in domesticated (sweet and red-fleshed) watermelon, but not
in citron melons (Citrullus amarus (PI296341-FR)), two SWEETlike sugar transporters (Sugars Will Eventually be Exported
Transporter (SWEET)) were highly expressed in developing redflesh of watermelon (but not rind), and their expression level was
correlated to the amount of fruit sugar, suggesting that they increase
fruit flesh sweetness by facilitating the active transmembrane
transport of sugars (Guo et al., 2015).
Work on watermelon has further identified a tonoplast sugar
transporter (ClTST2) that pumps sucrose, glucose and fructose
inside the fruit’s vacuoles (Ren et al., 2018). Cross-comparisons
across hundreds of Citrullus accessions spanning several species
revealed that increased expression of ClTST2 was a major event in
the domestication of the watermelon. ClTST2 is regulated by a
sugar-induced transcription factor called SUSIWM1, and a single
SNP in the tonoplast sugar transporter (ClTST2) has been fixed in
the sweet, domesticated watermelon, and underlies a sugar
accumulation quantitative trait locus (QTL) in watermelon (Ren
et al., 2018). Therefore, it appears that increased ClTST2 expression by enhanced binding efficiency of SUSIWM1 to the ClTST2
promoter was a key event increasing sugar content during the
domestication of the watermelon.
Altogether these data for honey melon and watermelon suggest
that increased sugar content resulted from selection on dozens of
genes altering sugar metabolism or transport.
3. Selection for larger fruits
In all 10 major Cucurbitaceae crops (Table 1), humans selected
for larger fruits. Fruit size is essentially controlled by three
processes in the ovary: cell differentiation (e.g. the definition of
the number of carpels), cell division and cell expansion. Carpel
number only varies from three to seven, with even very large
specimens of Cucurbita maxima only having five to seven carpels
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(Grumet & Colle, 2017). The increase in fruit size therefore
mostly involves shifts in the regulation of cell division and in cell
expansion. The transcriptional master regulators of the fruit size
gene networks are still unclear, but so far phytohormone-related
genes (auxin, cytokinins and gibberelins), microtubule-related
genes and cyclin-related genes appear to be the key players
controlling fruit size.
In watermelon, Citrullus lanatus, two MADS box genes similar
to the tomato ripening and expansion gene TAGL1 have been
characterised and are highly expressed during fruit expansion and
ripening, suggesting that they regulate both processes (Guo et al.,
2013). In cucumber, C. sativus, analysis of QTL identified a single
selective sweep with 19 genes, one of which encodes a cyclin
involved in cell proliferation (Qi et al., 2013). Another study
identified 12 QTLs for fruit size in this species that were linked to
different aspects of size, in particular length and width (Weng et al.,
2015), and that have been selected in different ways in the three
domestication directions of Cucumis sativus (Fig. 5 inset). Transcriptome analysis of cucumber revealed thousands of differentially
expressed genes, including many linked to microtubules and cyclins
(cell division) (Jiang et al., 2015). A single recessive gene,
spontaneous short fruit 1 (sf1), appears to regulate cucumber length
through auxin and cytokinin signalling (Wang et al., 2017).
Clearly the regulation of fruit size is a complex process, and
domestication has affected it in different ways (for instance, long
and thin Eurasian salad cucumbers vs short and thick East Asian
pickling cucumbers; Fig. 5), implying changes in the spatiotemporal fine-tuning of genes controlling cell division and
expansion. The world’s largest fruits are produced by Cucurbita
maxima cv Dill’s Atlantic Giant, with record fruits weighing
> 1000 kg. Despite the huge variation in fruit size and weight in
Cucurbitaceae crops and their close relatives, the regulatory control
underpinning these changes is not well understood. Functional
characterisation of candidate genes regulating cell division and
expansion in fruits is an exciting future research path. This
approach would pave the way for interesting comparisons of fleshy
fruit development across angiosperms of which the mechanisms are
currently almost exclusively known in tomato (Karlova et al.,
2014).
4. Seed traits
Relatively few Cucurbitaceae crops are cultivated for their seeds.
Most important economically are pumpkin seeds (Cucurbita pepo).
The Styrian pumpkin, C. pepo subsp. pepo var. styriaca, is a variety
that lost the seed testa following a single natural mutation in the
19th century (Teppner, 2004). Another cucurbit cultivated for its
seeds is the West African egusi melon, C. mucosospermus, which has
high nucleotide divergence from the domesticated watermelon
(C. lanatus) in loci controlling fatty acid metabolism in seeds (Guo
et al., 2013), consistent with the egusi melon’s role as a seed crop.
Mendelian genetics identified that a single recessive locus controlled the egusi seed type in Citrullus (Gusmini et al., 2004). In
China, a form of watermelon with fleshy reddish seeds is grown for
its seeds, which are toasted and eaten as a snack, and apparently this
use dates to AD 1250 (Mote, 1977).
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5. Selection for high carotenoid content
Several cucurbit crops accumulate b-carotene or lycopene, antioxidants that are highly beneficial to human health. Orange or red
fruit pulp due to naturally high carotenoid concentrations are also
found in wild species, for instance in the genera Momordica, Solena
and Trichosanthes. Studies of crops have focused on watermelon
and honey melon, in which the carotenoid accumulation results
from the regulation of several metabolic genes (Garcia-Mas et al.,
2012; Guo et al., 2013). In domesticated red-flesh watermelons,
two key genes of the carotenoid biosynthetic pathway – phytoene
synthase (PSY) and phytoene desaturase (PDS) – are upregulated
during fruit development (Guo et al., 2011, 2015).
Lycopene accumulation in watermelon has been linked to 19
transcription factors, with the accumulation mirrored by low
expression of lycopene cyclase, the enzyme that converts lycopene
into b-carotene (Grassi et al., 2013). Another lycopene-rich cucurbit is
the
Xishuangbanna
cucumber (Cucumis
sativus
var.
xishuangbannanensis, Renner, 2017), a form of cucumber domesticated c. 2500 years ago by the Hani ethnic group in China, Laos and
Vietnam, with high sugar and b-carotene content, similar to that of a
melon. Its orange flesh is due to a substitution of alanine to asparagine
at position 257 of the BCH1 gene, encoding a b-carotene hydroxylase
(Qi et al., 2013). This mutation leads to a nonfunctional b-carotene
hydroxylase that cannot convert b-carotene into zeaxanthin, leading to
an accumulation of b-carotene (Qi et al., 2013).
Building on these results, Zhang et al. (2017) reported that high
expression of a chromoplast-localised phosphate transporter
(ClPHT4;2) is needed for lycopene accumulation. While
ClPHT4;2 is present in both domesticated red-fleshed watermelon
and white-fleshed close relatives, it is expressed at a very low level in
white-fleshed watermelons. High expression of ClPHT4;2 relates
to the presence of key cis-acting elements in its promoters that
enables binding of sugar, abscisic acid and ethylene inducible
transcription factors ClbZIP1 and ClbZIP2. These cis-acting
elements are lacking in white-fleshed Citrullus (Zhang et al., 2017).
That ClbZIP1 and ClbZIP2 are sugar-inducible led Zhang et al.
(2017) to suggest that selection for sweetness and red colour
occurred concurrently in the watermelon. However, the fruits of
Citrullus lanatus subsp. cordophanus have white flesh combined
with a high sugar content (Ter-Avanesyn, 1966).
Tansley review
Review 13
locus (Shang et al., 2014; Zhou et al., 2016). Both honey melon
and watermelon were domesticated in Northeast Africa, perhaps in
the Upper Nile region of what is now Sudan, but honey melon was
also domesticated independently in Asia. Only a tiny subset of all
flowering plants has been brought into cultivation with certain
traits, such as an herbaceous habit or the ability to grow in disturbed
anthropogenic environments, apparently key reasons. For Cucurbitaceae, monoecy combined with an annual life cycle appears to
have been a factor (Fig. 1). Our review also highlights how the study
of crop domestication needs to combine genomic efforts with
traditional systematics and herbarium-verified specimens; this
approach is the most efficient way to infer species’ geographic
distributions and likely climatic adaptations.
Deciphering the domestication history of the major Cucurbitaceae crops will require further integration of population
genomics with collection-based research and archaeological samples. The huge array of useful traits and the large genetic diversity
found in the 23 minor cucurbit crops, as well as in wild progenitor
populations of major crops, opens up a number of exciting avenues
for de novo domestication, using CRISPR–Cas9 genome editing
(Zs€og€on et al., 2018). This approach would be especially useful for
plants like the watermelon, in which disease-resistance genes have
been lost during domestication (Guo et al., 2013).
Acknowledgements
We thank three reviewers for their comments, and Harry Paris,
Shaogui Guo and Bob Jarrett for discussion, and Oscar Alejandro
Perez-Escobar for generating the phylogeny shown in Fig. 4.
Financial support came from the DFG (grants RE 603/27-1 and
SCHA 1875/4-1) and the Elfriede and Franz Jakob Foundation for
research at the Botanical Garden Munich, Germany. GC is
supported by a Glasstone Research Fellowship and a Junior
Research Fellowship at Queen’s College, University of Oxford, UK.
ORCID
Guillaume Chomicki https://orcid.org/0000-0003-4547-6195
Susanne S. Renner https://orcid.org/0000-0003-3704-0703
Hanno Schaefer https://orcid.org/0000-0001-7231-3987
V. Conclusions
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