The mutation of CsSUN, an IQD family protein, is responsible for the short and fat fruit (sff) in cucumber (Cucumis sativus L)

Authors: ZHANG, ZHENGAO - Northwest A&f University; ZHANG, HAIQIANG - Northwest A&f University; LIU, JUNYAN - Northwest A&f University; CHEN, KANG - Northwest A&f University; WANG, YIXIN - Northwest A&f University; ZHANG, GAOYUAN - Gansu Agricultural Uiversity; LI, LIXIA - Shanxi Agriculture University; HONGZHONG, YUE - Gansu Academy Of Agricultural Sciences; Weng, Yiqun; LI, YUHONG - Northwest A&f University; CHEN, PENG - Northwest A&f University

Submitted to: Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/30/2024
Publication Date: 7/2/2024
Citation: Zhang, Z., Zhang, H., Liu, J., Chen, K., Wang, Y., Zhang, G., Li, L., Hongzhong, Y., Weng, Y., Li, Y., Chen, P. 2024. The mutation of CsSUN, an IQD family protein, is responsible for the short and fat fruit (sff) in cucumber (Cucumis sativus L). Plant Science. 346. https://doi.org/10.1016/j.plantsci.2024.112177.
DOI: https://doi.org/10.1016/j.plantsci.2024.112177

Interpretive Summary: Background Fruit shape of cucumber is an important agronomic trait, and mining regulatory genes, especially dominant ones, is vital for cucumber breeding. However, little is known on the genetic and molecular basis of fruit shape/size variation in cucumber fruit development. Findings In this study, we identified a short and fat fruit (sff) mutant from a cucumber line CCMC (wild type, WT). Compared to CCMC, the sff mutant plant exhibited reduced fruit length (shorter) and increased fruit dimeter (fatter). Genetic analysis found that the sff phenotype is controlled by a semi-dominant gene. With the map-based cloning strategy, the underlying gene was narrowed down to a 52.6 kb interval that contained a candidate gene that is responsible for the fruit shape variation. This gene encodes an IQD family protein, CsSUN. Two single nucleotide polymorphisms inside the CsSUN gene were sown to be responsible for the mutant fruit appearance. The function of this candidate gen in regulating fruit shape is confirmed by developing gene edited lines. The expression level of the CsSUN gene was reduced in the sff mutant fruit. Histological observations suggest that the sff mutant phenotype is due to increased transverse cell division and inhibited longitudinal cell division. Transcriptome analysis revealed that CsSUN significantly affected the expression of genes related to cell division, expansion, and auxin signal transduction. Significance This works reveals an important function of the SUN gene in shaping cucumber fruit. The work also provides a new tool for genetic manipulation of fruit size and shape in cucumber that may be useful for cucumber breeding.

Technical Abstract: The fruit shape of cucumber is an important agronomic trait, and mining regulatory genes, especially dominant ones, is vital for cucumber breeding. In this study, we identified a short and fat fruit mutant, named sff, from an EMS mutagenized population. Compared to the CCMC (WT), sff (MT) exhibited reduced fruit length and increased dimeter. Segregation analysis revealed that the sff phenotype is controlled by a semi-dominant single gene with dosage effects. Through map-based cloning, the SFF locus was narrowed down to a 52.6 kb interval with two SNPs (G651A and C1072T) in the second and third exons of CsaV3_1G039870, which encodes an IQD family protein, CsSUN. The G651A within the IQ domain of CsSUN was identified as the unique SNP among 114 cucumber accessions, and it was the primary cause of the functional alteration in CsSUN. By generating CsSUN knockout lines in cucumber, we confirmed that CsSUN was responsible for sff mutant phenotype. The CsSUN is localized to the plasma membrane. CsSUN exhibited the highest expression in the fruit with lower expression in sff compared to WT. Histological observations suggest that the sff mutant phenotype is due to increased transverse cell division and inhibited longitudinal cell division. Transcriptome analysis revealed that CsSUN significantly affected the expression of genes related to cell division, expansion, and auxin signal transduction. This study unveils CsSUN's crucial role in shaping cucumber fruit and offers novel insights for cucumber breeding.