Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses

<p>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<sub>3</sub> or C<sub>4<...

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Main Authors: Hughes, TE, Sedelnikova, O, Thomas, M, Langdale, J
Format: Journal article
Language:English
Published: Public Library of Science 2023
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author Hughes, TE
Sedelnikova, O
Thomas, M
Langdale, J
author_facet Hughes, TE
Sedelnikova, O
Thomas, M
Langdale, J
author_sort Hughes, TE
collection OXFORD
description <p>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<sub>3</sub> or C<sub>4</sub> photosynthesis. In both cases a series of parallel veins develops that extends from the leaf base to the tip but in ancestral C<sub>3</sub> species veins are separated by a greater number of intervening mesophyll cells than in derived C<sub>4</sub> 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<sub>4</sub> species maize, whereas it regulates the formation of stomata in the epidermal leaf layer in the C<sub>3</sub> species rice. Here we show that SCR is required for inner leaf patterning in the C<sub>4</sub> 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<sub>4</sub> but not C<sub>3</sub> 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<sub>4</sub> leaves.</p>
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spelling oxford-uuid:21e96e2c-274b-4164-8cc0-b8970ead8cc52023-07-04T10:37:33ZMutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grassesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:21e96e2c-274b-4164-8cc0-b8970ead8cc5EnglishSymplectic ElementsPublic Library of Science2023Hughes, TESedelnikova, OThomas, MLangdale, J<p>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<sub>3</sub> or C<sub>4</sub> photosynthesis. In both cases a series of parallel veins develops that extends from the leaf base to the tip but in ancestral C<sub>3</sub> species veins are separated by a greater number of intervening mesophyll cells than in derived C<sub>4</sub> 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<sub>4</sub> species maize, whereas it regulates the formation of stomata in the epidermal leaf layer in the C<sub>3</sub> species rice. Here we show that SCR is required for inner leaf patterning in the C<sub>4</sub> 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<sub>4</sub> but not C<sub>3</sub> 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<sub>4</sub> leaves.</p>
spellingShingle Hughes, TE
Sedelnikova, O
Thomas, M
Langdale, J
Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title_full Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title_fullStr Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title_full_unstemmed Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title_short Mutations in NAKED-ENDOSPERM IDD genes reveal functional interactions with SCARECROW during leaf patterning in C4 grasses
title_sort mutations in naked endosperm idd genes reveal functional interactions with scarecrow during leaf patterning in c4 grasses
work_keys_str_mv AT hugheste mutationsinnakedendospermiddgenesrevealfunctionalinteractionswithscarecrowduringleafpatterninginc4grasses
AT sedelnikovao mutationsinnakedendospermiddgenesrevealfunctionalinteractionswithscarecrowduringleafpatterninginc4grasses
AT thomasm mutationsinnakedendospermiddgenesrevealfunctionalinteractionswithscarecrowduringleafpatterninginc4grasses
AT langdalej mutationsinnakedendospermiddgenesrevealfunctionalinteractionswithscarecrowduringleafpatterninginc4grasses