Summary
Leaf shape evolution in angiosperms is reviewed from an evolutionary developmental (evo/devo) viewpoint. Leaves have evolved as photosynthetic organs in land plants, while leaves in some angiosperms have lost their photosynthetic role, e.g., in some cacti, saprophytes/mycoheterotrophs, and parasitic plants. Although the roles are the same among leaves, their morphologies and developmental systems vary significantly, in part because of the need to maximize their photosynthetic efficiency for survival under particular environmental constraints. An example is the narrow leaves of the rheophyte plants located along river banks where frequent flooding occurs. Narrow leaves are less efficient at absorbing sunlight than are leaves with wider blades; however, they can withstand the destructive force of the water flow in full flood. In contrast, in some xerophytic epiphytes, the narrow leaves are effective at catching water from fog. Narrow leaf blade formation is also present in submerged amphibious plants, likely an adaptation to the underwater conditions. The leaf index, i.e., the ratio of leaf length to width, is regulated by several genetic factors, mutations of which may be driving the evolution of leaf shape. However, not all leaf shapes can be explained by environmental adaptation. For example, data on the relationship between leaf shape diversification and environmental habitats in terms of thermo regulation remain controversial.
In contrast, understanding of the genetic/cellular mechanisms underlying leaf blade shape is increasing. Leaf blade organogenesis is governed by adaxial/abaxial identities, in which the plate meristem, responsible for flat leaf blade development, is activated along the interface between the adaxial and abaxial domains. Thus, some morphological diversity in leaves can be partly attributed to changes in the adaxial/abaxial patterning. For example, unifacial leaves, which have only an abaxial identity in the leaf blade, develop into stick-like or terete forms. They can stand vertically and thus live in densely populated areas, unlike plants with bifacial leaves which extend, in most cases, horizontally. Interestingly, some unifacial leaves are flat or ensiform, as seen in the genera Iris and Juncus. In such cases, since the plate meristem is not available, they rely on thickening growth to create flat lamina from the terete primordia. Lotus-like or peltate leaves are also derived from partial alterations in the adaxial/abaxial patterning; however, the pitcher leaves of carnivorous plants, once considered an extreme deformation of the peltate leaves, result from local alterations in cell division. In compound leaves, the major genetic regulatory components are shared with those of serrated leaf margins. The proportion of serrated-leaf species in any particular habitat precisely correlates with the average air temperature, and thus serration mechanisms are likely linked to physiological adaptations to the external environment. The evolution of determinate and indeterminate leaves in angiosperms is also discussed. While leaves are usually determinate and discarded periodically, some species develop indeterminate leaves, with some looking like twigs or lateral branches and functioning as twigs. Some are simple leaves and have an intermediate nature between a leaf and a shoot. We also see the evolution of leaf-like, photosynthetic organs. Some plants develop cladodes, which are modified lateral shoots that resemble leaves. Molecular analysis revealed that recruitment of dorsiventral control mechanisms in leaves has resulted in lateral shoots changing into leaf-like cladodes in the genus Asparagus. All of the above can be interpreted from an evo/devo viewpoint, but the question of why such great diversification occurred in angiosperm leaves remains.
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Abbreviations
- AN:
-
ANGUSTIFOLIA
- AN3:
-
ANGUSTIFOLIA3
- ARF:
-
AUXIN RESPONSE FACTOR
- AS1, AS2:
-
ASYMMETRIC LEAVES 1, ASYMMETRIC LEAVES 2
- ATGIF1:
-
Arabidopsis thaliana GIF1
- AtGRF:
-
Arabidopsis thaliana GRF
- BOP:
-
BLADE-ON-PETIOLE
- CIN-TCP:
-
CINCINNATA-class-TCP
- CRC:
-
CRABS CLAW
- CtBP/BARS:
-
C-terminal Binding Protein/ /BFA–ADP-Ribosylation Substrate
- CUC:
-
CUP-SHAPED COTYLEDON
- DL:
-
DROOPING LEAF
- ETT:
-
ETTIN
- FLO:
-
FLORICAULA
- evo/devo:
-
evolutionary developmental biology
- GA:
-
gibberellic acid
- GIF:
-
GRF-INTERACTING FACTOR
- GLK:
-
GOLDEN2-LIKE
- GRF:
-
GROWTH REGULATING FACTOR
- HD-ZipIII:
-
HOMEODOMAIN LEUCINE ZIPPER Class III
- KAN:
-
KANADI
- KNOX:
-
KNOTTED-LIKE HOMEOBOX
- KNOX I:
-
Class I KNOX
- L1:
-
Layer 1
- LFY:
-
LEAFY
- LNG:
-
LONGIFOLIA
- miR:
-
micro RNA
- NGA:
-
NGATHA
- oli:
-
oligocellula
- PIN1:
-
PIN-FORMED 1
- PHAN:
-
PHANTASTICA
- PRS:
-
PRESSED FLOWER
- RCO:
-
REDUCED COMPLEXITY
- ROT3:
-
ROTUNDIFOLIA 3
- RTFL/DVL:
-
ROTUNDOFOLIA FOUR-LIKE/DEVIL
- SAM:
-
shoot apical meristem
- STM:
-
SHOOT MERISTEMLESS
- tasiR:
-
trans-acting siRNA
- TCP:
-
TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL NUCLEAR ANTIGEN FACTOR1 transcription factor
- WOX1:
-
WUSCHEL-LIKE HOMEODOMAIN 1
- xs:
-
extra-small sisters
- YAB:
-
YABBY
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Acknowledgments
This work was supported by the Bio-Next project in NINS, the Japan Society for the Promotion of Science (Grants-in-Aid for Creative Scientific Research and Scientific Research A), The Ministry of Education, Culture, Sports, Science and Technology, Japan (Scientific Research on Priority Areas and Scientific Research on Innovative Areas No. 25113002). In addition, the author thanks reviewers of the manuscript who helped him to polish it. Dr. Hiroyuki Koga of the University of Tokyo also kindly checked the final version of the manuscript.
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Tsukaya, H. (2018). A Consideration of Leaf Shape Evolution in the Context of the Primary Function of the Leaf as a Photosynthetic Organ. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_1
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