期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：3
DOI：10.1073/pnas.2108641119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Nitrogen fixation is economically important in agriculture. Enhancing nodulation in soybean can greatly enhance nitrogen fixation efficiency. Nodule formation in legumes starts with cortical cell divisions in the root. Despite the discovery of the Nod factors and plant hormones that are involved, it remains unclear how cortical cell division is spatiotemporally regulated. Here we provide evidence that soybean has acquired two
SHORT-ROOT (
SHR) paralogs during evolution, which are specifically induced in the early stage of nodule organogenesis. These
SHR homologs can activate the expression of early nodulin genes and enhance cytokinin signaling and form part of a multilevel regulatory network to activate D-type cyclins during nodulation. Our results provide insight into the mechanisms of nodule organogenesis in soybean.
Nitrogen fixation in soybean takes place in root nodules that arise from de novo cell divisions in the root cortex. Although several early nodulin genes have been identified, the mechanism behind the stimulation of cortical cell division during nodulation has not been fully resolved. Here we provide evidence that two paralogs of soybean SHORT-ROOT (GmSHR) play vital roles in soybean nodulation. Expression of
GmSHR4 and
GmSHR5 (
GmSHR4/5) is induced in cortical cells at the beginning of nodulation, when the first cell divisions occur. The expression level of
GmSHR4/5 is positively associated with cortical cell division and nodulation. Knockdown of GmSHR5 inhibits cell division in outer cortical layers during nodulation. Knockdown of both paralogs disrupts the cell division throughout the cortex, resulting in poorly organized nodule primordia with delayed vascular tissue formation. GmSHR4/5 function by enhancing cytokinin signaling and activating early nodulin genes. Interestingly, D-type cyclins act downstream of GmSHR4/5, and GmSHR4/5 form a feedforward loop regulating D-type cyclins. Overexpression of D-type cyclins in soybean roots also enhanced nodulation. Collectively, we conclude that the GmSHR4/5-mediated pathway represents a vital module that triggers cytokinin signaling and activates D-type cyclins during nodulation in soybean.
