Redundant SCARECROW genes pattern distinct cell layers in roots and leaves of maize.

Thomas E. Hughes,Jane A. Langdale,Olga V. Sedelnikova,Hao Wu,Philip W. Becraft

doi:10.1242/dev.177543

Thomas E. Hughes, Jane A. Langdale + Show 3 more

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https://doi.org/10.1242/dev.177543

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Abstract

ABSTRACTThe highly efficient C4 photosynthetic pathway is facilitated by ‘Kranz’ leaf anatomy. In Kranz leaves, closely spaced veins are encircled by concentric layers of photosynthetic bundle sheath (inner) and mesophyll (outer) cells. Here, we demonstrate that, in the C4 monocot maize, Kranz patterning is regulated by redundant function of SCARECROW 1 (ZmSCR1) and a previously uncharacterized homeologue: ZmSCR1h. ZmSCR1 and ZmSCR1h transcripts accumulate in ground meristem cells of developing leaf primordia and in Zmscr1;Zmscr1h mutant leaves, most veins are separated by one rather than two mesophyll cells; many veins have sclerenchyma above and/or below instead of mesophyll cells; and supernumerary bundle sheath cells develop. The mutant defects are unified by compromised mesophyll cell development. In addition to Kranz defects, Zmscr1;Zmscr1h mutants fail to form an organized endodermal layer in the root. Collectively, these data indicate that ZmSCR1 and ZmSCR1h redundantly regulate cell-type patterning in both the leaves and roots of maize. Leaf and root pathways are distinguished, however, by the cell layer in which they operate – mesophyll at a two-cell distance from leaf veins versus endodermis immediately adjacent to root vasculature.

Highlights

The C4 photosynthetic pathway, which is responsible for around 21% of global primary productivity despite being found in only ~3% of plant species (Ehleringer et al, 1997; Sage et al, 2011), is underpinned by a specialized leaf anatomy known as Kranz
Given that the root endodermis and the leaf bundle sheath (BS) are considered analogous cell types (Esau, 1943; Nelson, 2011), it is possible that an ancestral SCR patterning function was recruited in the leaf rather than the root in maize, but the subtle phenotype reported in leaves of Zmscr1 mutants precludes an understanding of the precise role played during Kranz development
The maize SCR duplicates reside on syntenic regions of chromosomes 4 (ZmSCR1) and 2 (ZmSCR1h), and have previously been annotated as likely homeolog gene pairs that arose through the recent maize whole genome duplication (Schnable et al, 2011)

Summary

Introduction

The C4 photosynthetic pathway, which is responsible for around 21% of global primary productivity despite being found in only ~3% of plant species (Ehleringer et al, 1997; Sage et al, 2011), is underpinned by a specialized leaf anatomy known as Kranz (the German word for wreath) (reviewed in Sedelnikova et al, 2018). Given the higher yields found in many C4 plants, there are ongoing attempts to engineer the C4 pathway into C3 crops (Hibberd et al, 2008; von Caemmerer et al, 2012; Wang et al, 2016), such attempts require a far better understanding of how vein spacing and leaf cell fate is regulated in C4 species. Given that the root endodermis and the leaf BS are considered analogous cell types (Esau, 1943; Nelson, 2011), it is possible that an ancestral SCR patterning function was recruited in the leaf rather than the root in maize, but the subtle phenotype reported in leaves of Zmscr mutants precludes an understanding of the precise role played during Kranz development

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