A functional allele of CsFUL1 regulates fruit length through repressing CsSUP and inhibiting auxin transport in cucumber

Authors: ZHAO, JIANYU - China Agricultural University; JIANG, LI - China Agricultural University; CHE, GEN - China Agricultural University; LI, YANQIANG - China Agricultural University; PAN, YUPENG - University Of Wisconsin; ZHAO, WENSHENG - China Agricultural University; ZHONG, YANTING - China Agricultural University; DING, YAN - China Agricultural University; YAN, SHUANGSHUANG - China Agricultural University; SUN, CHENGZHEN - China Agricultural University; Weng, Yiqun; ZHANG, XIAOLAN - China Agricultural University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/29/2019
Publication Date: 4/12/2019
Citation: Zhao, J., Jiang, L., Che, G., Li, Y., Pan, Y., Zhao, W., Zhong, Y., Ding, Y., Yan, S., Sun, C., Weng, Y., Zhang, X. 2019. A functional allele of CsFUL1 regulates fruit length through repressing CsSUP and inhibiting auxin transport in cucumber. The Plant Cell. 31:1289–1307. https://doi.org/10.1105/tpc.18.00905.
DOI: https://doi.org/10.1105/tpc.18.00905

Interpretive Summary: Cucumber is an important vegetable crop. The fruit length is a horticultural important trait affecting fruit yield and quality since each market class has unique requirements for fruit size and diameter at commercial harvest stage. A better understanding of the regulatory mechanism of fruit length variation may help modulate cucumber fruit growth in cucumber breeding. However, little is known in this regard. In this study, we found an important player, CsFUL1 in control of fruit elongation in cucumber. CsFUL is a MADS-box type transfactor gene, which is a negative regulator for fruit elongation in cucumber. The expression of the CsFUL1 gene is high flowers and fruits, and its level is negatively correlated with fruit length in different cucumber lines. This gene seems to be the target of selection during the breeding history of North China fresh market (Chinese Long) cucumbers. Increase of expression of the CsFUL1 in transgenic plants reduces fruit length. The CsFUL1 regulates fruit length through two pathways: one by inhibiting a gene for auxin transport and the other by interacting with other MADS-box genes to suppress cell division and cell expansion. This is important because findings from this study identified novel mechanisms in cucumber to regulate fruit development. This work provides an important target gene for plant breeders for the manipulation of fruit elongation in cucumber breeding. This is important for developmental biologists who have an interest in understanding molecular mechanisms of fruit development.

Technical Abstract: Cucumber (Cucumis sativus L.) is an important vegetable crop bearing fleshy pepo fruits that harvested immature. The fruit length is one of the most important horticultural traits that directly determines fruit yield and affects fruit quality, but the regulatory mechanism of fruit length variation remains elusive. Here we found that FRUITFULL-like MADS-box gene CsFUL1 functions as a key repressor for fruit length regulation in cucumber. The expression of CsFUL1 is highly enriched in flowers and fruits, and negatively correlated with fruit length in different cucumber lines. The CSFUL1 gene seems to be the target of diversifying selection for the Chinese Long cucumbers that typically set long-fruits. Ectopic expression of CsFUL1 was unable to rescue the indehiscent fruit phenotype of ful-1 in Arabidopsis. Overexpression of CsFUL1 resulted in increased floral organs and reduced fruit length, whereas knockdown of CsFUL1 led to elongated fruit in cucumber. Transcriptome and biochemical analyses showed that CsFUL1 regulates fruit length through two pathways: one by inhibiting the PIN-FORWED (PIN1/7)-mediated auxin transport and thus downregulates auxin related genes in the fruit, and the other by forming a tetramer with other MADS-box genes to repress the CsSUP-mediated cell division and cell expansion. In addition, we found that CsFUL1 promotes locule number variation through the well known CsWUS-CsCLV pathway. Our findings uncover the regulatory commonality and specificity during development of different fruit types, and provide an important candidate gene to manipulation of fruit elongation in cucumber breeding.