Effective range of non-cell autonomous activator and inhibitor peptides specifying plant stomatal patterning

Zeng, Scott; Lo, Emily K.W.; Hazelton, B. J.; Morales, M. F.; Torii, Keiko U.

doi:10.1242/dev.192237

Cited by 16 publications

(14 citation statements)

References 47 publications

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“…In arabidopsis, both extrinsic EPF peptide signalling and intrinsic polarity pathways downregulate SPCH–SCRMs via the activation of MAPK cascades ( Herrmann and Torii, 2021 ). Indeed, a tissue mosaic study using Cre–Lox recombination-dependent EPF1 overexpression sectors showed that secreted extrinsic signals influence adjacent cells as well as those within a range of a few cells ( Zeng et al , 2020 ). The intrinsic polarity component, BASL (BREAKING OF ASSYMMETRY IN THE STOMATAL LINEAGE), specifies the SLGC fate to one of the two daughter cells generated by the asymmetric cell division of a meristemoid ( Dong et al , 2009 ).…”

Section: Stomatal Development In the Context Of Epidermal Patterningmentioning

confidence: 99%

Stomatal development in the context of epidermal tissues

Torii

2021

Annals of Botany

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Background Stomata are adjustable pores on the surface of plant shoots for efficient gas exchange and water control. The presence of stomata is essential for plant growth and survival, and the evolution of stomata is considered as a key developmental innovation of the land plants, allowing colonization on land from aquatic environments some 450 million years ago. In the past two decades, molecular genetic studies using the model plant Arabidopsis thaliana identified key genes and signalling modules that regulate stomatal development: master-regulatory transcription factors that orchestrate cell-state transitions and peptide-receptor signal transduction pathways, which, together, enforce proper patterning of stomata within the epidermis. Studies in diverse plant species, ranging from bryophytes to angiosperm grasses, have begun to unravel the conservation and uniqueness of the core modules in stomatal development. Scope Here, I review the mechanisms of stomatal development in the context of epidermal tissue patterning. First, I introduce the core regulatory mechanisms of stomatal patterning and differentiation in the model species Arabidopsis thaliana. Subsequently, experimental evidence is presented supporting the idea that different cell types within the leaf epidermis, namely stomata, hydathodes pores, pavement cells, and trichomes, either share developmental origins or mutually influence each other’s gene regulatory circuits during development. Emphasis is taken on extrinsic and intrinsic signals regulating the balance between stomata and pavement cells, specifically by controlling the fate of Stomatal-Lineage Ground Cells (SLGCs) to remain within the stomatal-cell lineage or differentiate into pavement cells. Finally, I discuss the influence of inter-tissue-layer communication between the epidermis and underlying mesophyll/vascular tissues on stomatal differentiation. Understanding the dynamic behaviors of stomatal precursor cells and their differentiation in the broader context of tissue and organ development may help design plants tailored for optimal growth and productivity in specific agricultural applications and a changing environment.

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Section: Stomatal Development In the Context Of Epidermal Patterningmentioning

confidence: 99%

Stomatal development in the context of epidermal tissues

Torii

2021

Annals of Botany

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“…The mature form of STOMAGEN contains 45 amino acids and positively regulates stomatal density in Arabidopsis [ 23 , 27 , 44 ], while EPF1 and EPF2 negatively regulate stomatal density [ 42 , 45 , 46 , 47 ]. In this study, PagSTOMAGEN from 84K poplar was homologous with STOMAGEN in Arabidopsis , rice , and Populus trichocarpa ( Figure 1 A,B), and its mature form contained 43 amino acids ( Figure 1 C).…”

Section: Discussionmentioning

confidence: 99%

Overexpression of PagSTOMAGEN, a Positive Regulator of Stomatal Density, Promotes Vegetative Growth in Poplar

Xia

Ling

et al. 2022

IJMS

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Poplar is an important fast-growing tree, and its photosynthetic capacity directly affects its vegetative growth. Stomatal density is closely related to photosynthetic capacity and growth characteristics in plants. Here, we isolated PagSTOMAGEN from the hybrid poplar (Populus alba × Populus glandulosa) clone 84K and investigated its biological function in vegetative growth. PagSTOMAGEN was expressed predominantly in young tissues and localized in the plasma membrane. Compared with wild-type 84K poplars, PagSTOMAGEN-overexpressing plants displayed an increased plant height, leaf area, internode number, basal diameter, biomass, IAA content, IPR content, and stomatal density. Higher stomatal density improved the net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate in transgenic poplar. The differential expression of genes related to stomatal development showed a diverged influence of PagSTOMAGEN at different stages of stomatal development. Finally, transcriptomic analysis showed that PagSTOMAGEN affected vegetative growth by affecting the expression of photosynthesis and plant hormone-related genes (such as SAUR75, PQL2, PSBX, ERF1, GNC, GRF5, and ARF11). Taken together, our data indicate that PagSTOMAGEN could positively regulate stomatal density and increase the photosynthetic rate and plant hormone content, thereby promoting vegetative growth in poplar. Our study is of great significance for understanding the relationship between stoma, photosynthesis, and yield breeding in poplar.

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“…In their absence, veins are formed in regions between already specified veins, resulting in the runs of fused veins observed in maize and setaria scr;nkd mutants. This mechanism may be analogous to the lateral inhibition mechanism that patterns trichomes and stomata on the leaf surface (Schellmann et al, 2002; Torii, 2012; Zeng et al, 2020), whereby the fused veins represent a clustering phenotype caused by absence of the inhibitor. Because SCR and NKD do not accumulate in developing veins, in this scenario it is likely that they would interpret an inhibitory signal emanating from adjacent specified veins.…”

Section: Discussionmentioning

confidence: 99%

Mutations inNAKED-ENDOSPERMIDD genes reveal functional interactions withSCARECROWand a maternal influence on leaf patterning in C₄grasses

Hughes

Sedelnikova

Thomas

et al. 2022

Preprint

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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 C3 or C4 photosynthesis. In both cases a series of parallel veins develops that extends from the leaf base to the tip but in ancestral C3 species veins are separated by a greater number of intervening mesophyll cells than in derived C4 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 C4 species maize, whereas it regulates the formation of stomata in the epidermal leaf layer in the C3 species rice. Here we show that SCR is required for inner leaf patterning in the C4 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 C4 but not C3 grasses. Finally, we identified a maternal effect in maize whereby maternally derived NKD can affect patterning of cells in leaf primordia that are initiated during embryogenesis. Together our results provide insight into the evolution of cell patterning in grass leaves, demonstrate a novel patterning role for IDD genes in C4 leaves and suggest that NKD can influence embryonic leaf development non-cell autonomously from the surrounding maternal tissue.

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Effective range of non-cell autonomous activator and inhibitor peptides specifying plant stomatal patterning

Cited by 16 publications

References 47 publications

Stomatal development in the context of epidermal tissues

Stomatal development in the context of epidermal tissues

Overexpression of PagSTOMAGEN, a Positive Regulator of Stomatal Density, Promotes Vegetative Growth in Poplar

Mutations inNAKED-ENDOSPERMIDD genes reveal functional interactions withSCARECROWand a maternal influence on leaf patterning in C₄grasses

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Effective range of non-cell autonomous activator and inhibitor peptides specifying plant stomatal patterning

Cited by 16 publications

References 47 publications

Stomatal development in the context of epidermal tissues

Stomatal development in the context of epidermal tissues

Overexpression of PagSTOMAGEN, a Positive Regulator of Stomatal Density, Promotes Vegetative Growth in Poplar

Mutations inNAKED-ENDOSPERMIDD genes reveal functional interactions withSCARECROWand a maternal influence on leaf patterning in C4grasses

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Mutations inNAKED-ENDOSPERMIDD genes reveal functional interactions withSCARECROWand a maternal influence on leaf patterning in C₄grasses