Temperature-sensitive male sterility in rice determined by the roles of AGO1d in reproductive phasiRNA biogenesis and function

Temperature-sensitive male sterility in rice determined by the roles of AGO1d in reproductive phasiRNA biogenesis and function
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DOI:
10.1111/nph.18446
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发表时间:
2022-09-17
期刊:
影响因子:
9.4
通讯作者:
Fei, Qili
Fei, Qili
中科院分区:
生物学1区
文献类型:
--
作者:
Shi, Chuanlin;Zhang, Jie;Fei, Qili

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阶段性次生siRNAs广泛存在于开花植物的生殖组织中,具有时空特异性。然而,与phasiRNAs相关的ArgAerte(AGO)蛋白及其miRNA触发器仍然难以捉摸。在这里,通过组织学和高通量测序分析,我们发现水稻AGO1d在减数分裂前和减数分裂期间在花药壁细胞中特异表达,与miR2118和miR2275都相关,介导phasiRNA的生物发生。AGO1d优先与miR2118触发的21-核苷酸(NT)phasiRNA结合,5‘端尿苷,提示在phasiRNA的生物发生和功能中具有双重作用。AGO1d的缺失会导致21-和24-nt的phasiRNAs减少,并导致温度敏感型雄性不育。在较低的温度下,该突变体的花药在花粉形成过程中主要表现为绒毡层细胞过多,淀粉积累很少,这可能是由于细胞代谢失调所致。这些结果揭示了AGO1d在低温下水稻花药发育中的重要作用,并证明了AGO蛋白在生殖PhsiRNA生物发生和功能中的协调作用。
Phased secondary siRNAs (phasiRNAs) are broadly present in the reproductive tissues of flowering plants, with spatial-temporal specificity. However, the ARGONAUTE (AGO) proteins associated with phasiRNAs and their miRNA triggers remain elusive. Here, through histological and high-throughput sequencing analyses, we show that rice AGO1d, which is specifically expressed in anther wall cells before and during meiosis, associates with both miR2118 and miR2275 to mediate phasiRNA biogenesis. AGO1d preferentially binds to miR2118-triggered 21-nucleotide (nt) phasiRNAs with a 5 '-terminal uridine, suggesting a dual role in phasiRNA biogenesis and function. Depletion of AGO1d causes a reduction of 21- and 24-nt phasiRNAs and temperature-sensitive male sterility. At lower temperatures, anthers of the ago1d mutant predominantly show excessive tapetal cells with little starch accumulation during pollen formation, possibly caused by the dysregulation of cell metabolism. These results uncover an essential role of AGO1d in rice anther development at lower temperatures and demonstrate coordinative roles of AGO proteins during reproductive phasiRNA biogenesis and function.