Gene regulatory network of carpel number variation in cucumber

Authors: CHE, GEN - China Agricultural University; GU, REN - China Agricultural University; ZHAO, JIANYU - China Agricultural University; LIU, XIAOFENG - China Agricultural University; CHENG, ZHIHUA - China Agricultural University; WANG, ZHONGYI - China Agricultural University; LIU, RENYI - Fujian Agricultural & Forestry University; YAN, LIYAN - Hebei University; Weng, Yiqun; ZHANG, XIAOLAN - China Agricultural University; ZI, HAILING - Shanghai Institutes For Biological Sciences; SONG, XIAOFEI - Hebei University; SHEN, JUNJUN - China Agricultural University

Submitted to: Development
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/5/2020
Publication Date: 4/6/2020
Citation: Che, G., Gu, R., Zhao, J., Liu, X., Cheng, Z., Wang, Z., Liu, R., Yan, L., Weng, Y., Zhang, X., Zi, H., Song, X., Shen, J. 2020. Gene regulatory network of carpel number variation in cucumber. Development. 147(7). https://doi.org/10.1242/dev.184788.
DOI: https://doi.org/10.1242/dev.184788

Interpretive Summary: Background information: Cucumber is an important vegetable crop. Cucumber fruit size and shape are important fruit yield and quality attributes. Many factors including carpel numbers affect fruit size and shape. In plants, the WUSCHEL (WUS)-CLAVATA3 (CLV3) pathway plays important roles stem apical meristem (SAM) maintenance and floral organ development, but how the CLV3 gene affect carpel development is not well known. Findings: In this study, we found that the expression of cucumber CLV3 was negatively correlated with carpel number in cucumber cultivars. Reduced expression of it led to increased number of petals and carpels, whereas increased expression of WUS resulted in more sepals, petals and carpels. This suggests that CLV3 and WUS function as a negative and a positive regulator for carpel number variation, respectively. Increase the expression of CsFUL1 that involves in fruit length regulation resulted in more petals and carpels. We identified additional players participating in carpel number variation in cucumber. Why is it important? Findings from this study identified the genetic/molecular mechanisms in cucumber to regulate carpel development during fruit growth. Such knowledge provides better understanding of fruit development in cucumber at the molecular level. Who cares? Plant geneticists and molecular biologists who have interests in understanding molecular mechanisms of fruit development in cucumber.

Technical Abstract: The WUSCHEL (WUS)-CLAVATA3 (CLV3) pathway genes play essential role in shoot apical meristem (SAM) maintenance and floral organ development, and under intense selection during crop domestication. The carpel number (CN) is an important fruit trait affecting fruit shape, size, and internal quality in cucumber, but the molecular mechanism remains elusive. Here, we found that the expression of CsCLV3 was negatively correlated with carpel number in cucumber cultivars. Knockdown of CsCLV3 led to increased number of petals and carpels, whereas overexpression of CsWUS resulted in more sepals, petals and carpels, suggesting that CsCLV3 and CsWUS function as a negative and a positive regulator for carpel number variation, respectively. Interestingly, the expression region of CsCLV3 overlaps with CsWUS in the basal domain of the SAM in cucumber. Overexpression of CsFUL1, a FRUITFULL-like MADS-box gene involved in fruit length regulation, resulted in more petals and carpels. CsFUL1 can directly bind to CsWUS promoter to stimulate its expression. Further, we found that auxin participates in carpel number variation in cucumber through physical interaction of AUXIN RESPONSE FACTOR 14 (CsARF14) with CsWUS. Therefore, we identified a gene regulatory pathway involving CsCLV3, CsWUS, CsFUL1 and CsARF14 in determining carpel number variation in an important vegetable crop-cucumber.