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Title: SHORT HYPOCOTYL 1 encodes a SMARCA3-like chromatin remodeling factor regulating elongation

Author
item B0, KAILIANG - University Of Wisconsin
item WANG, H - University Of Wisconsin
item PAN, Y - University Of Wisconsin
item BEHERA, TUSAR - University Of Wisconsin
item PANDEY, S - University Of Wisconsin
item WEN, C - University Of Wisconsin
item WANG, Y - University Of Wisconsin
item Simon, Philipp
item LI, Y - University Of Wisconsin
item CHEN, JINFENG - University Of Wisconsin
item Weng, Yiqun

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/22/2016
Publication Date: 10/1/2016
Publication URL: https://handle.nal.usda.gov/10113/63259
Citation: Bo, K., Wang, H., Pan, Y., Behera, T.K., Pandey, S., Wen, C., Wang, Y., Simon, P.W., Li, Y., Chen, J., Weng, Y. 2016. SHORT HYPOCOTYL 1 encodes a SMARCA3-like chromatin remodeling factor regulating elongation. Plant Physiology. 172(2):1273-1292. doi: 10.1104/pp.16.00501.

Interpretive Summary: In Arabidopsis, the UVR8-mediated signaling pathway is employed to attain UVB protection and acclimation to deal with low dosage UVB (LDUVB)-induced stresses. In this study, we identified SHORT HYPOCOTYL1 (SH1) in cucumber which regulates LDUVB-dependent hypocotyl elongation by recruiting the cucumber UVR8 signaling pathway. We showed that hypocotyl elongation in cucumbers carrying the recessive sh1 allele was LDUVB-insensitive. Map-based cloning revealed that Sh1 encoded a human SMARCA3-like chromatin remodeling transcription factor. The allele frequency and distribution pattern at this locus among natural populations supported the wild cucumber origin of sh1 for local adaptation, which was under selection during domestication. The cultivated cucumber carries predominantly the Sh1 allele; the sh1 allele is nearly fixed in the semi-wild Xishuangbanna cucumber, and the wild cucumber population is largely at HW equilibrium for the alleles. The SH1 protein sequence was highly conserved among eukaryotic organisms, but its function in regulating hypocotyl elongation was unique to cucumber. While Sh1 expression was inhibited by LDUVB, its transcript abundance was highly correlated with hypocotyl elongation rate and the expression level of cell elongation-related genes. Expression profiling of key regulator genes in the UVR8 signaling pathway revealed significant differential expression of CsHY5 between two near isogenic lines of Sh1 under UVB-free white light, where SH1 and CsHY5 acted antagonistically. A working model was proposed in which the SH1 regulates LDUVB-dependent hypocotyl elongation in cucumber by modulating the UVR8 signaling pathway through changing the chromatin states thus the accessibility of CsHY5 to promoters of LDUVB-responsive genes for hypocotyl elongation.

Technical Abstract: Understanding the mechanisms and control of hypocotyl elongation is important for greenhouse vegetable crop production. In this study, we identified SHORT HYPOCOTYL1 (SH1) in cucumber which regulates low-dosage ultraviolet B (LDUVB)-dependent hypocotyl elongation by recruiting the cucumber UVR8 signaling pathway. We showed that hypocotyl elongation in cucumbers carrying the recessive sh1 allele was LDUVB-insensitive. We found that Sh1 encoded a human SMARCA3-like chromatin remodeling transcription factor. The allele frequency and distribution pattern at this locus among natural populations supported the wild cucumber origin of sh1 for local adaptation, which was under selection during domestication. The cultivated cucumber carries predominantly the Sh1 allele; the sh1 allele is nearly fixed in the semi-wild Xishuangbanna cucumber, and the wild cucumber population is largely at HW equilibrium for the alleles. The SH1 protein sequence was highly conserved among eukaryotic organisms, but its function in regulating hypocotyl elongation was unique to cucumber. While Sh1 expression was inhibited by LDUVB, its transcript abundance was highly correlated with hypocotyl elongation rate and the expression level of cell elongation-related genes. We provided evidence to support our hypothesis that the SH1 protein regulates LDUVB-dependent hypocotyl elongation in cucumber by modulating the UVR8 signaling pathway through changing the chromatin states thus the accessibility of CsHY5 to promoters of LDUVB-responsive genes for hypocotyl elongation. We also discussed potential use of this gene in cucumber breeding for production in protected environments.