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Abstract Grass leaves develop from a ring of primordial initial cells within the periphery of the shoot apical meristem, a pool of organogenic stem cells that generates all of the organs of the plant shoot. At maturity, the grass leaf is a flattened, strap-like organ comprising a proximal supportive sheath surrounding the stem and a distal photosynthetic blade. The sheath and blade are partitioned by a hinge-like auricle and the ligule, a fringe of epidermally derived tissue that grows from the adaxial (top) leaf surface. Together, the ligule and auricle comprise morphological novelties that are specific to grass leaves. Understanding how the planar outgrowth of grass leaves and their adjoining ligules is genetically controlled can yield insight into their evolutionary origins. Here we use single-cell RNA-sequencing analyses to identify a ‘rim’ cell type present at the margins of maize leaf primordia. Cells in the leaf rim have a distinctive identity and share transcriptional signatures with proliferating ligule cells, suggesting that a shared developmental genetic programme patterns both leaves and ligules. Moreover, we show that rim function is regulated by genetically redundant Wuschel-like homeobox3 (WOX3) transcription factors. Higher-order mutations in maizeWox3genes greatly reduce leaf width and disrupt ligule outgrowth and patterning. Together, these findings illustrate the generalizable use of a rim domain during planar growth of maize leaves and ligules, and suggest a parsimonious model for the homology of the grass ligule as a distal extension of the leaf sheath margin.
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Network analyses identify a transcriptomic proximodistal prepattern in the maize leaf primordium
Summary The formation of developmental boundaries is a common feature of multicellular plants and animals, and impacts the initiation, structure and function of all organs. Maize leaves comprise a proximal sheath that encloses the stem, and a distal photosynthetic blade that projects away from the plant axis. An epidermally derived ligule and a joint‐like auricle develop at the blade/sheath boundary of maize leaves. Mutations disturbing the ligule/auricle region disrupt leaf patterning and impact plant architecture, yet it is unclear how this developmental boundary is established.Targeted microdissection followed by transcriptomic analyses of young leaf primordia were utilized to construct a co‐expression network associated with development of the blade/sheath boundary.Evidence is presented for proximodistal gradients of gene expression that establish a prepatterned transcriptomic boundary in young leaf primordia, before the morphological initiation of the blade/sheath boundary in older leaves.This work presents a conceptual model for spatiotemporal patterning of proximodistal leaf domains, and provides a rich resource of candidate gene interactions for future investigations of the mechanisms of blade/sheath boundary formation in maize.
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- Award ID(s):
- 1710973
- PAR ID:
- 10452953
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 230
- Issue:
- 1
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 218-227
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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