Cell type boundaries organize plant development

Caggiano, Monica Pia; Yu, Xiulian; Bhatia, Neha; Larsson, Anna-Maria; Ram, Hasthi; Ohno, Carolyn; Sappl, Pia G.; Meyerowitz, Elliot M.; Jönsson, Henrik; Heisler, Marcus G.

doi:10.7554/elife.27421

Cited by 116 publications

(145 citation statements)

References 69 publications

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“…However, more recent work in Arabidopsis has determined that microsurgical wounding depletes auxin from the SAM, which causes the down‐regulation of HD‐ZIPIII expression. This loss of HD‐ZIPIII in the SAM subsequently activates the ectopic expression of abaxializing KAN genes in adaxial domains of the shoot apex (Caggiano et al ., ). Thus, in this model, wound‐induced disruption of an adaxial–abaxial prepattern in the incipient, but as yet unelaborated, leaf primordium leads to the formation of unifacial, abaxialized leaves.…”

Section: Flat Laminar Growth: Patterning and Coordination Of Adaxial–mentioning

confidence: 97%

“…Light energy is efficiently captured by flat surfaces. Current models predict that the pre‐primordial juxtaposition of adaxial (top) and abaxial (bottom) domains organizes a new axis of expansive mediolateral growth from the SAM PZ, to give rise to the flattened lamina of bifacial leaves (Waites & Hudson, ; Caggiano et al ., ). In their landmark paper inspired by studies of the development of flattened wings in Drosophila melanogaster (Diaz‐Benjumea & Cohen, ; Williams et al ., ), Waites and Hudson examined the abaxialized, radial, adult leaves of the Antirrhinum mutant phantastica ( PHAN ) and extended these animal models to describe the relationship between adaxial–abaxial and mediolateral patterning in plant leaves (Waites & Hudson, ).…”

Section: Flat Laminar Growth: Patterning and Coordination Of Adaxial–mentioning

confidence: 99%

“…The monophyletic monocots diverged from their eudicot relatives quite early in angiosperm evolution (Hertweck et al ., ), although details of their evolutionary relationships are blurred by evolutionary convergences among the nearly 300 000 species within the two orders (Christenhusz & Byng, ). This review focuses on the comparative ontogeny of monocot and eudicot foliar leaves, which develop from the shoot apical meristem (SAM) and are dorsiventrally asymmetric from their inception (Roth, ; Hagemann, ; Caggiano et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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On the mechanisms of development in monocot and eudicot leaves

Conklin

Strable

et al. 2018

New Phytologist

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Contents Summary I. Introduction II. Leaf zones in monocot and eudicot leaves III. Monocot and eudicot leaf initiation: differences in degree and timing, but not kind IV. Reticulate and parallel venation: extending the model? V. Flat laminar growth: patterning and coordination of adaxial-abaxial and mediolateral axes VI. Stipules and ligules: ontogeny of primordial elaborations VII. Leaf architecture VIII. Stomatal development: shared and diverged mechanisms for making epidermal pores IX. Conclusion Acknowledgements References SUMMARY: Comparisons of concepts in monocot and eudicot leaf development are presented, with attention to the morphologies and mechanisms separating these angiosperm lineages. Monocot and eudicot leaves are distinguished by the differential elaborations of upper and lower leaf zones, the formation of sheathing/nonsheathing leaf bases and vasculature patterning. We propose that monocot and eudicot leaves undergo expansion of mediolateral domains at different times in ontogeny, directly impacting features such as venation and leaf bases. Furthermore, lineage-specific mechanisms in compound leaf development are discussed. Although models for the homologies of enigmatic tissues, such as ligules and stipules, are proposed, tests of these hypotheses are rare. Likewise, comparisons of stomatal development are limited to Arabidopsis and a few grasses. Future studies may investigate correlations in the ontogenies of parallel venation and linear stomatal files in monocots, and the reticulate patterning of veins and dispersed stoma in eudicots. Although many fundamental mechanisms of leaf development are shared in eudicots and monocots, variations in the timing, degree and duration of these ontogenetic events may contribute to key differences in morphology. We anticipate that the incorporation of an ever-expanding number of sequenced genomes will enrich our understanding of the developmental mechanisms generating eudicot and monocot leaves.

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Section: Flat Laminar Growth: Patterning and Coordination Of Adaxial–mentioning

confidence: 97%

Section: Flat Laminar Growth: Patterning and Coordination Of Adaxial–mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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On the mechanisms of development in monocot and eudicot leaves

Conklin

Strable

et al. 2018

New Phytologist

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“…These include LAM1 in Nicotiana sylvestris (Lin et al., ), STF in Medicago truncatula (Tadege et al., ), narrow sheath1 and 2 in maize (Nardmann, Ji, Werr, & Scanlon, ), and narrow leaf2 and 3 in rice (Ishiwata et al., ). In Arabidopsis, the closely related WOX1 and PRS (aka WOX3 ) genes have described roles in leaf development (Nakata et al., ), during which their expression is induced by auxin (Caggiano et al., ). prs wox1 leaves display reduced blade outgrowth and fewer margin cell files (Nakata et al., ) while PRS over‐expressor lines show an increase in leaf margin cell file number (Supporting Information Figure ), indicating that PRS and WOX1 promote blade outgrowth and margin cell file formation.…”

Section: Discussionmentioning

confidence: 99%

Peptide signaling molecules CLE5 and CLE6 affect Arabidopsis leaf shape downstream of leaf patterning transcription factors and auxin

et al. 2018

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Intercellular signaling mediated by small peptides is critical to coordinate organ formation in animals, but whether extracellular polypeptides play similar roles in plants is unknown. Here we describe a role in Arabidopsis leaf development for two members of the CLAVATA 3/ ESR ‐ RELATED peptide family, CLE 5 and CLE 6, which lie adjacent to each other on chromosome 2. Uniquely among the CLE genes, CLE 5 and CLE 6 are expressed specifically at the base of developing leaves and floral organs, adjacent to the boundary with the shoot apical meristem. During vegetative development CLE 5 and CLE 6 transcription is regulated by the leaf patterning transcription factors BLADE ‐ ON ‐ PETIOLE 1 ( BOP 1) and ASYMMETRIC LEAVES 2 ( AS 2), as well as by the WUSCHEL ‐ RELATED HOMEOBOX ( WOX ) transcription factors WOX 1 and PRESSED FLOWER ( PRS ). Moreover, CLE 5 and CLE 6 transcript levels are differentially regulated in various genetic backgrounds by the phytohormone auxin. Analysis of loss‐of‐function mutations generated by genome engineering reveals that CLE 5 and CLE 6 independently and together have subtle effects on rosette leaf shape. Our study indicates that the CLE 5 and CLE 6 peptides function downstream of leaf patterning factors and phytohormones to modulate the final leaf morphology.

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“…The alternative proposal that adaxially expressed HDZIPIII genes limit the auxin response, restricting WOX1 and PRS expression to the middle domain of the leaf (Bhatia et al ) contradicts experimental findings, including their own. PRS is a target of auxin signaling (Caggiano et al ; Guan et al ). The expression of the HDZIPIII gene REVOLUTA ( REV ) substantially overlaps with that of PRS (Figure S7), as shown in a previous report by the Heisler group (Figure 4D in Caggiano et al ).…”

mentioning

confidence: 99%