|LIU, XIAOFENG - China Agricultural University|
|NING, KANG - China Agricultural University|
|CHE, GEN - China Agricultural University|
|YAN, SHUANGSHUANG - China Agricultural University|
|HAN, LIJIE - China Agricultural University|
|GU, RAN - China Agricultural University|
|LI, ZHENG - Northwest Agricultural & Forestry University|
|ZHANG, XIAOLAN - China Agricultural University|
Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2018
Publication Date: 3/31/2018
Citation: Liu, X., Ning, K., Che, G., Yan, S., Han, L., Gu, R., Li, Z., Weng, Y., Zhang, X. 2018. CsSPL functions as an adaptor between HD-ZIP III and CsWUS transcription factors regulating anther and ovule development in cucumber. Plant Journal. 94(3):535-547. https://doi.org.10.1111/tpj.13877.
Interpretive Summary: In plant reproductive development, anthers and ovules produce male and female spores, respectively. The SPOROCYTELESS (SPL) gene is a critical gene for spore generation, but its function in cucumber has never been explored, how it is regulated is also unknown. In this study, we characterized the function of cucumber SPL gene. SPL was expressed specifically in the developing anthers and ovules. Reduced expression of SPL leads to reduced male and female fertility with malformed pollens and suppressed ovule development. Several other genes are identified that work together with SPL to control male and female fertility. From this work, we discovered a new regulatory pathway in which SPL acts as a bridge between other genes to determine sex organ development in cucumber. This work also found the important roles of the plant hormone auxin in developing anthers and ovaries. Our work fills a knowledge gap in understanding the roles of the SPL gene affecting the male and female fertility in cucumber.
Technical Abstract: Anthers and ovules are the sex organs that produce male and female spores, respectively. The SPOROCYTELESS (SPL)/NOZZLE (NZZ) encodes a nuclear protein controlling the sporogenesis in sex organs. However, the function of SPL in unisexual plants has never been explored, and the upstream regulators of SPL remain elusive. Here, we characterized the SPL homolog gene CsSPL in cucumber, an important vegetable crop with unisexual flowers. CsSPL was expressed specifically in the developing anthers and ovules. Knockdown of CsSPL led to reduced male and female fertility with malformed pollens and suppressed ovule development. CsSPL directly interacts with CsWUS (WUSCHEL) in nucellus and YABBY family genes in integuments. HD-ZIP III gene CsPHB (PHABULOSA) is expressed specifically in the nucellus and promotes CsSPL expression by binding to CsSPL promoter. Hence, we uncovered a new regulatory pathway in which CsSPL acting as the adaptor between HD-ZIP III genes and CsWUS during sex organ development in cucumber. In addition, auxin content was decreased in the CsSPL knockdown plants, and auxin was enriched in developing anthers and ovules. Further analyses showed that CsSPL was positively regulated by AUXIN RESPONSE FACTOR (CsARF13), and CsSPL stimulates the expression of CsARF3 during reproductive organ development.