ODR1/AtSDR4L alleviates osmotic stress-induced germination arrest via ABA-dependent negative feedback on ABA biosynthesis

ODR1/AtSDR4L通过ABA依赖的ABA生物合成负反馈来缓解渗透胁迫引起的种子萌发停滞。

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Abstract

BACKGROUND: To optimize offspring seed survival in fluctuating environments, seed plants have evolved two key adaptive strategies, seed dormancy under favorable conditions and germination arrest under stress, to control germination timing. The phytohormone abscisic acid acts as a master regulator in both processes, exerting precise control over its endogenous levels and signaling to fine-tune this seed-seedling transition. Previously, we identified ODR1 as a key seed dormancy regulator: it negatively modulates seed dormancy by suppressing ABA accumulation during seed development via inhibiting bHLH57-dependent transcriptional activation of the ABA biosynthesis genes NCED6/9. However, whether ODR1 also modulates seed germination under stress conditions remains unknown. RESULTS: Here, we showed that loss of ODR1 function arrested seed germination under osmotic stress, while specific overexpression of ODR1 in odr1 mutant seeds rescued this osmotic germination arrest. Osmotic stress induced and maintained high ODR1 expression, but this induction was reduced in the ABA biosynthesis-deficient mutant nced6/9 and ABA signaling mutants abi3-1, abi4-t, and abi5-8, indicating ABA dependence of ODR1 induction. In odr1 mutants, 8 out of 12 key ABA biosynthesis genes were significantly upregulated. ChIP-seq data analysis revealed an ODR1 binding peak in the promoter of the ABA biosynthesis gene ABA1. Specific overexpression of ODR1 in odr1 mutant seeds notably rescued the upregulated ABA1 expression, confirming the repression of ABA1 by ODR1. Furthermore, ABA content was significantly increased in germinating seeds of odr1 mutant, and exogenous application of fluridone, an ABA biosynthesis inhibitor, effectively rescued their germination arrest, linking the phenotype to excessive ABA accumulation. CONCLUSIONS: These results reveal a novel role of ODR1 in osmotic stress-induced germination arrest: ODR1 is induced by osmotic stress via an ABA-dependent pathway and in turn limits ABA accumulation via repressing the expression of ABA biosynthesis genes, thereby alleviating germination arrest under stress. Together, we demonstrate that ODR1 coordinates germination timing via ABA-dependent negative feedback regulation of ABA biosynthesis during both dormancy establishment and osmotic stress responses. This mechanism addresses the critical question of how plants fine-tune ABA signaling to balance survival and germination in variable environments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-025-07570-y.

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