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Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses
Leaves comprise a number of different cell-types that are patterned in the context of either the epidermal or inner cell layers. In grass leaves, two distinct anatomies develop in the inner leaf tissues depending on whether the leaf carries out C(3) or C(4) photosynthesis. In both cases a series of...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138192/ https://www.ncbi.nlm.nih.gov/pubmed/37068119 http://dx.doi.org/10.1371/journal.pgen.1010715 |
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author | Hughes, Thomas E. Sedelnikova, Olga Thomas, Mimi Langdale, Jane A. |
author_facet | Hughes, Thomas E. Sedelnikova, Olga Thomas, Mimi Langdale, Jane A. |
author_sort | Hughes, Thomas E. |
collection | PubMed |
description | Leaves comprise a number of different cell-types that are patterned in the context of either the epidermal or inner cell layers. In grass leaves, two distinct anatomies develop in the inner leaf tissues depending on whether the leaf carries out C(3) or C(4) photosynthesis. In both cases a series of parallel veins develops that extends from the leaf base to the tip but in ancestral C(3) species veins are separated by a greater number of intervening mesophyll cells than in derived C(4) species. We have previously demonstrated that the GRAS transcription factor SCARECROW (SCR) regulates the number of photosynthetic mesophyll cells that form between veins in the leaves of the C(4) species maize, whereas it regulates the formation of stomata in the epidermal leaf layer in the C(3) species rice. Here we show that SCR is required for inner leaf patterning in the C(4) species Setaria viridis but in this species the presumed ancestral stomatal patterning role is also retained. Through a comparative mutant analysis between maize, setaria and rice we further demonstrate that loss of NAKED-ENDOSPERM (NKD) INDETERMINATE DOMAIN (IDD) protein function exacerbates loss of function scr phenotypes in the inner leaf tissues of maize and setaria but not rice. Specifically, in both setaria and maize, scr;nkd mutants exhibit an increased proportion of fused veins with no intervening mesophyll cells. Thus, combined action of SCR and NKD may control how many mesophyll cells are specified between veins in the leaves of C(4) but not C(3) grasses. Together our results provide insight into the evolution of cell patterning in grass leaves and demonstrate a novel patterning role for IDD genes in C(4) leaves. |
format | Online Article Text |
id | pubmed-10138192 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-101381922023-04-28 Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses Hughes, Thomas E. Sedelnikova, Olga Thomas, Mimi Langdale, Jane A. PLoS Genet Research Article Leaves comprise a number of different cell-types that are patterned in the context of either the epidermal or inner cell layers. In grass leaves, two distinct anatomies develop in the inner leaf tissues depending on whether the leaf carries out C(3) or C(4) photosynthesis. In both cases a series of parallel veins develops that extends from the leaf base to the tip but in ancestral C(3) species veins are separated by a greater number of intervening mesophyll cells than in derived C(4) species. We have previously demonstrated that the GRAS transcription factor SCARECROW (SCR) regulates the number of photosynthetic mesophyll cells that form between veins in the leaves of the C(4) species maize, whereas it regulates the formation of stomata in the epidermal leaf layer in the C(3) species rice. Here we show that SCR is required for inner leaf patterning in the C(4) species Setaria viridis but in this species the presumed ancestral stomatal patterning role is also retained. Through a comparative mutant analysis between maize, setaria and rice we further demonstrate that loss of NAKED-ENDOSPERM (NKD) INDETERMINATE DOMAIN (IDD) protein function exacerbates loss of function scr phenotypes in the inner leaf tissues of maize and setaria but not rice. Specifically, in both setaria and maize, scr;nkd mutants exhibit an increased proportion of fused veins with no intervening mesophyll cells. Thus, combined action of SCR and NKD may control how many mesophyll cells are specified between veins in the leaves of C(4) but not C(3) grasses. Together our results provide insight into the evolution of cell patterning in grass leaves and demonstrate a novel patterning role for IDD genes in C(4) leaves. Public Library of Science 2023-04-17 /pmc/articles/PMC10138192/ /pubmed/37068119 http://dx.doi.org/10.1371/journal.pgen.1010715 Text en © 2023 Hughes et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Hughes, Thomas E. Sedelnikova, Olga Thomas, Mimi Langdale, Jane A. Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title | Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title_full | Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title_fullStr | Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title_full_unstemmed | Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title_short | Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C(4) grasses |
title_sort | mutations in naked-endosperm idd genes reveal functional interactions with scarecrow during leaf patterning in c(4) grasses |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138192/ https://www.ncbi.nlm.nih.gov/pubmed/37068119 http://dx.doi.org/10.1371/journal.pgen.1010715 |
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