Leaf morphogenesis: The multifaceted roles of mechanics

Guo, Kexin; Huang, Changjin; Miao, Yansong; Cosgrove, Daniel J.; Hsia, Karen

doi:10.1016/j.molp.2022.05.015

Cited by 24 publications

(12 citation statements)

References 201 publications

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“…Additionally, plant leaves are sites for photosynthesis, thus serving as the most important tissue supplying energy for plant growth and development (Song et al, 2015;Guo et al, 2022). Leaf primordia cells originate from shoot apical meristem (SAM) and evolve into distinct morphological shapes for environmental adaptation (Kierzkowski et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Simultaneous Analysis of Single-nucleus Transcriptome and Chromatin Accessibility Unveils the Mechanisms of Leaf Cell Development in Arachis hypogaea L.

Líu

Deng

et al. 2023

Preprint

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Plant cell development is an asynchronous process that is governed by multiple layers of gene regulation. However, the correlation between transcriptome and chromatin regulatory events in an allotetraploid species at the single-cell resolution has not been widely studied. Herein, we employed fluorescence-activated nuclei sorting to isolate single nuclei and simultaneously investigate the transcriptome (snRNA-seq) and chromatin accessibility (snATAC-seq) landscapes in the same leaf single-cell of Arachis hypogaea. A total of 5,930 cells with 10,793 expressed genes were classified into 17 cell-clusters and 5,315 chromatin fragments were enriched to target 26,083 genes in the snATAC-seq landscape. The developmental trajectory revealed a conserved ethylene-AP2 module in leaf cell differentiation and provided novel insight for mesophyll and vascular cell development. Additionally, dual-omics described the epidermal progenitor cell development trajectory, primordium and palisade cells were able to convert into spongy cells, and bundle sheath cells developed earlier than other vascular-cells. Further cell-cycle analysis demonstrated that cytokinin biosynthesis promotes mesophyll cell genome replication and lipid pathway participates in guard cell development. snRNA-seq identified that the AT-hook transcription factor AhAHL11promotes leaf area growth by modulating auxin content, but snATAC-seq identified AhBHLH143 displaying contrasting results by repressing leaf development via the jasmonic acid pathway in ectopically expressed Arabidopsis. Conclusively, our study demonstrates that snRNA-seq combined with snATAC-seq is an effective platform for exploring the association between chromatin regulatory events and transcriptional activity across diverse cell types in peanut leaves. The broad application of this approach will enable significant advances in the functional research of tissue growth and development in plant species. Plant cell development is an asynchronous process that is governed by multiple layers of gene regulation. However, the correlation between transcriptome and chromatin regulatory events in an allotetraploid species at the single-cell resolution has not been widely studied. Herein, we employed fluorescence-activated nuclei sorting to isolate single nuclei and simultaneously investigate the transcriptome (snRNA-seq) and chromatin accessibility (snATAC-seq) landscapes in the same leaf single-cell of peanut. Totally 5,930 cells with 10,793 expressed genes were classified into 17 cell-clusters and 5,315 chromatin fragments were enriched to target 26,083 genes in the snATAC-seq landscape. Developmental trajectory revealed a conserved ethylene-AP2 module in leaf cell differentiation and provided novel insights for mesophyll and vascular cells development. Further ell-cycle demonstrated that cytokinin promotes mesophyll-cell genome replication and lipid pathway participates in guard cell development. snRNA-seq identified AhAHL11 promotes leaf area growth by modulating auxin content, but snATAC-seq identified AhBHLH143 repressing leaf development via jasmonic acid pathway. Conclusively, snRNA-seq combined with snATAC-seq is an effective platform for exploring the association between chromatin regulatory events and transcriptional activity across diverse cell-types. The broad application of this approach will enable significant advances in the functional research of tissue growth and development in plant species.

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Section: Introductionmentioning

confidence: 99%

Simultaneous Analysis of Single-nucleus Transcriptome and Chromatin Accessibility Unveils the Mechanisms of Leaf Cell Development in Arachis hypogaea L.

Líu

Deng

et al. 2023

Preprint

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“…The formation of folds is important in many systems, including the gut (Savin et al , 2011; Shyer et al , 2013), the wrinkles of the brain (Llinares‐Benadero & Borrell, 2019), the development of the Drosophila wing (Tozluoğlu et al , 2019), and others (see Nelson, 2016, for a review). Buckling due to differential growth is a key mechanism in the determination of leaf shapes (reviewed in Guo et al , 2022). We do not discuss this in this review, but mechanical forces in general play an important role in plant morphogenesis (see Sampathkumar, 2020, for a review).…”

Section: Introductionmentioning

confidence: 99%

Forceful patterning: theoretical principles of mechanochemical pattern formation

Rombouts,

Elliott,

Erzberger

2023

EMBO Reports

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Biological pattern formation is essential for generating and maintaining spatial structures from the scale of a single cell to tissues and even collections of organisms. Besides biochemical interactions, there is an important role for mechanical and geometrical features in the generation of patterns. We review the theoretical principles underlying different types of mechanochemical pattern formation across spatial scales and levels of biological organization.

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“…Plants usually grow in a linear or circumferential orientation; however, some plants show twisted (Kerwin, 2021), spiral, and circled growth (Zheng et al, 2018). These phenotypic traits are alterations caused by increased environmental selection pressure (Max et al, 2021;Alexandra et al, 2019) or heritable variations (Guo et al, 2022). Some genes involved in twisted growth have been identified using model plants, includ-ingSmSPR1 , WAVY (Masashi et al, 2010), spiral1 , spiral2 (Stéphane et al, 2019),lefty1 , lefty2 (Siripong et al, 2002), and CSI1 (Martin et al, 2012.…”

Section: Introductionmentioning

confidence: 99%

The cellulose--lignin balance affects the twisted growth of Yunnan pine trunk

cui

Liu

et al. 2022

Preprint

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It is a debate whether trunk twisting belongs to environmental alteration or genetic variation. Through a diallel cross experiment, we first determined that trunk twisting of Yunnan pines was controlled by recessive genes. Anatomical analysis identified that straight and twisty types differed in xylem and phloem. RNA-seq of materials enriched by laser microdissection revealed three genes involved in auxin signal transduction, photosynthesis, and sucrose metabolism, namely ARF, POR, and CBH. These genes were co-expressed at different growth stages of twisty types, and among them, ARF is crucial regulating trunk twisting formation. The enzyme activities involved in sucrose metabolism, carbon fixation, and glycolysis were significantly increased after exogenous auxin was added to twisty types. When auxin signal transduction inhibitor (auxinole) and transport inhibitor (TIBA) were added, the plant height and related pathways were more obviously reduced in straight types. ARF can not only downregulate POR to block chlorophyll synthesis but also allows abundant sucrose to synthesize cellulose. Nevertheless, due to downregulated CBH expression and abnormal cellulolysis, cellulose accumulates and the lignin content decreases, eventually making the trunk highly prone to twisted growth. This study suggests that ARF can be vital in trunk shape screening during the early growth of Yunnan pines.

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Leaf morphogenesis: The multifaceted roles of mechanics

Cited by 24 publications

References 201 publications

Simultaneous Analysis of Single-nucleus Transcriptome and Chromatin Accessibility Unveils the Mechanisms of Leaf Cell Development in Arachis hypogaea L.

Simultaneous Analysis of Single-nucleus Transcriptome and Chromatin Accessibility Unveils the Mechanisms of Leaf Cell Development in Arachis hypogaea L.

Forceful patterning: theoretical principles of mechanochemical pattern formation

The cellulose--lignin balance affects the twisted growth of Yunnan pine trunk

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