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Biphasic control of cell expansion by auxin coordinates etiolated seedling development.

ABSTRACT: Seedling emergence is critical for food security. It requires rapid hypocotyl elongation and apical hook formation, both of which are mediated by regulated cell expansion. How these events are coordinated in etiolated seedlings is unclear. Here, we show that biphasic control of cell expansion by the phytohormone auxin underlies this process. Shortly after germination, high auxin levels restrain elongation. This provides a temporal window for apical hook formation, involving a gravity-induced auxin maximum on the eventual concave side of the hook. This auxin maximum induces PP2C.D1 expression, leading to asymmetrical H⁺-ATPase activity across the hypocotyl that contributes to the differential cell elongation underlying hook development. Subsequently, auxin concentrations decline acropetally and switch from restraining to promoting elongation, thereby driving hypocotyl elongation. Our findings demonstrate how differential auxin concentrations throughout the hypocotyl coordinate etiolated development, leading to successful soil emergence.

SUBMITTER: Du M

PROVIDER: S-EPMC8754305 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Biphasic control of cell expansion by auxin coordinates etiolated seedling development.

Du Minmin M Bou Daher Firas F Liu Yuanyuan Y Steward Andrew A Tillmann Molly M Zhang Xiaoyue X Wong Jeh Haur JH Ren Hong H Cohen Jerry D JD Li Chuanyou C Gray William M WM

Science advances 20220112 2

Seedling emergence is critical for food security. It requires rapid hypocotyl elongation and apical hook formation, both of which are mediated by regulated cell expansion. How these events are coordinated in etiolated seedlings is unclear. Here, we show that biphasic control of cell expansion by the phytohormone auxin underlies this process. Shortly after germination, high auxin levels restrain elongation. This provides a temporal window for apical hook formation, involving a gravity-induced aux ...[more]

PMID: 35020423

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Project description:To better understand light regulation of C(4) plant maize development, we investigated dynamic proteomic differences between green seedlings (control), etiolated seedlings, and etiolated seedlings illuminated for 6 or 12 h using a label-free quantitative proteomics approach based on nanoscale ultraperformance liquid chromatography-ESI-MS(E). Among more than 400 proteins identified, 73 were significantly altered during etiolated maize seedling greening. Of these 73 proteins, 25 were identified as membrane proteins that seldom had been identified with two-dimensional electrophoresis methods, indicating the power of our label-free method for membrane protein identification; 31 were related to light reactions of chlorophyll biosynthesis, photosynthesis, and photosynthetic carbon assimilation. The expression of photosystem II subunits was highly sensitive to light; most of them were not identified in etiolated maize seedlings but drastically increased upon light exposure, indicating that the complex process of biogenesis of the photosynthetic apparatus correlates with the transition from a dark-grown to a light-grown morphology. However, transcriptional analysis indicated that most transcripts encoding these proteins were not regulated by light. In contrast, the levels of mRNAs and proteins for enzymes involved in carbon assimilation were tightly regulated by light. Additionally phosphoenolpyruvate carboxykinase, the key enzyme of the phosphoenolpyruvate carboxykinase C(4) pathway, was more tightly regulated by light than the key enzymes of the NADP-malic enzyme C(4) pathway. Furthermore phosphoenolpyruvate carboxylase 1C, which was originally reported to be specifically expressed in roots, was also identified in this study; expression of this enzyme was more sensitive to light than its isoforms. Taken together, these results represent a comprehensive dynamic protein profile and light-regulated network of C(4) plants for etiolated seedling greening and provide a basis for further study of the mechanism of gene function and regulation in light-induced development of C(4) plants.

Project description:The phytohormone brassinosteroid (BR) regulate various developmental and physiological processes in plants. However, the function of BR during early seedling development stage in rapeseed is largely unknown. To understand the effects of exogenous BR during early seedling development, the ZS11 and BR-INSENSITIVE (bin2) mutants were treated with BR before seed sowing and seed germination stage under 16/8 hours light/dark cycle. The phenotype results indicated that BR promotes only seedling establishment but not seed germination stage in ZS11, while no function in bin2 mutants. Since BRs play a crucial role in regulation of developmental transition between growth in the dark (skotomorphogenesis) and growth in the light (photomorphogenesis), the ZS11 and bin2 mutants were treated with BR under continuous light and dark. The BR treatment also showed the same functions as 16/8 hours light/dark cycle. To understand the function of BR on expression levels, the differentially expressed genes (DEGs) and differentially expressed metabolites (DEMs) between mock- and BR-treated seedlings were explored. A total of 234 significantly DEGs were identified between the mock- and BR-treated groups by transcriptomic analyses. These DEGs were markedly enriched in BR biosynthesis, pentose and glucuronate interconversions and plant hormone signal transduction pathways. Meanwhile, a total of 145 DEMs were identified through metabolomics analyses, with a significant enrichment in lipid substances. Interestingly, some genes and metabolites associated with auxin pathway were identified, which exhibited up-regulation in both DEGs and DEMs after BR treatment. Subsequently, functional enrichment analyses revealed that the majority of DEGs and DEMs were primarily enriched in ascorbate and aldehyde metabolism, arginine and proline metabolism, tryptophan metabolism (the main route for auxin synthesis) and cyanogenic amino acid metabolism. Furthermore, it was found that glutamate was up-regulated in nitrogen metabolism, glyoxylate and dicarboxylate metabolism, and arginine and proline metabolism pathways. These indicated that the glutamate signaling pathway was a key regulatory pathway for exogenous BR to induce seedling establishment. These evidence implied that exogenous BR treatment lead to up-regulation of auxin-related genes expression, then promoted seedling establishment in rapeseed.

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Biphasic control of cell expansion by auxin coordinates etiolated seedling development.

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Biphasic control of cell expansion by auxin coordinates etiolated seedling development.

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