SHORT HYPOCOTYL1 Encodes a SMARCA3-Like Chromatin Remodeling Factor Regulating Elongation 1[OPEN] Kailiang Bo, Hui Wang, Yupeng Pan, Tusar K. Behera, Sudhakar Pandey, Changlong Wen, Yuhui Wang, Philipp W. Simon, Yuhong Li, Jinfeng Chen*, and Yiqun Weng* Horticulture Department, University of Wisconsin, Madison, Wisconsin 53706 (K.B., Y.P., Y.Wa., P.W.S., Y.We.); Horticulture College, Nanjing Agricultural University, Nanjing 210095, China (K.B., J.C.); Horticulture College, Northwest A&F University, Yangling 712100, China (H.W., Y.P., Y.L.); Division of Vegetable Science, Indian Agricultural Research Institute, New Delhi 10012, India (T.K.B.); Division of Crop Improvement, Indian Council of Agricultural Research-Indian Institute of Vegetable Research, Varanasi, Uttar Pradesh 221305, India (S.P.); Beijing Vegetable Research Center and National Engineering Research Center for Vegetables, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, China (C.W.); and Vegetable Crops Research Unit, United States Department of Agriculture Agricultural Research Service, Madison, Wisconsin 53706 (P.W.S., Y.We.) ORCID IDs: 0000-0002-6053-443X (K.B.); 0000-0003-4662-601X (Y.P.); 0000-0002-4690-6778 (J.C.); 0000-0001-9457-2234 (Y.We.). In Arabidopsis (Arabidopsis thaliana), the UVR8-mediated signaling pathway is employed to attain UVB protection and acclimation to deal with low-dosage UVB (LDUVB)-induced stresses. Here, we identified SHORT HYPOCOTYL1 (SH1) in cucumber (Cucumis sativus), which regulates LDUVB-dependent hypocotyl elongation by modulating the UVR8 signaling pathway. We showed that hypocotyl elongation in cucumbers carrying the recessive sh1 allele was LDUVB insensitive and that Sh1 encoded a human SMARCA3-like chromatin remodeling 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 semiwild Xishuangbanna cucumber, and the wild cucumber population is largely at Hardy-Weinberg equilibrium for the two alleles. The SH1 protein sequence was highly conserved among eukaryotic organisms, but its regulation of hypocotyl elongation in cucumber seems to be a novel function. 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 regulators in the UVR8 signaling pathway revealed signi ficant differential expression of CsHY5 between two near isogenic lines of Sh1. Sh1 and CsHY5 acted antagonistically at transcriptional level. A working model was proposed in which Sh1 regulates LDUVB-dependent hypocotyl elongation in cucumber through changing the chromatin states and thus the accessibility of CsHY5 in the UVR8 signaling pathway to promoters of LDUVB-responsive genes for hypocotyl elongation. The hypocotyl of dicotyledonous plants is the em- bryonic stem connecting the two embryonic leaves (cot- yledons) and the primary root (radicle). The hypocotyl, which has a relatively simple architecture (Scheres et al., 1994), is a very plastic organ, strongly influenced by both external and internal cues known to regulate cell elongation, such as light, gravity, temperature, and hormones. In Arabidopsis (Arabidopsis thaliana), after germination, hypocotyl growth relies mainly on lon- gitudinal cell elongation rather than cell divisions; its length can increase by more than 10-fold (Gendreau et al., 1997). The morphological simplicity, growth behavior, availability of mutants, and ease of pheno- typing of mutants of this organ makes it a model for understanding the mechanism of cell elongation and various biological events that participate in its control (Gendreau et al., 1997; Vandenbussche et al., 2005; Boron and Vissenberg, 2014). In nature, the development of germinated seeds starts under soil cover; the seedling undergoing skoto- morphogenic growth has a very long hypocotyl, which allows quick attaining of light and de-etiolation after 1 This work was supported by a United States Department of Ag- riculture Specialty Crop Research Initiative grant (SCRI, project no. 2011-51181-30661) to Y.We. The work in Y.L.’s lab was supported by the National Natural Science Foundation of China (31171955 and 31471891). J.C.’s work was supported by the National Natural Science Foundation of China (31430075). * Address correspondence to yiqun.weng@wisc.edu and jfchen@ njau.edu.cn. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy de- scribed in the Instructions for Authors (www.plantphysiol.org) is: Yiqun Weng (yiqun.weng@wisc.edu). K.B. performed majority of the research and conducted data anal- ysis; Y.We. designed and supervised the experiments and partici- pated in data analysis; H.W. and Y.L. conducted yeast two-hybrid experiments; Y.P. performed genetic mapping in the WI7167 3 WI7200 population; T.K.B. and S.P. collected genotypic and pheno- typic data for wild cucumbers; Y.Wa. performed GWAS analysis of the data; C.W. performed SNP genotyping of the C. hystrix and XIS accessions; J.C., Y.L., and P.W.S. participated in supervising the ex- periments; Y.We. and K.B. wrote this article with input from the co- authors; all authors reviewed and approved this submission. [OPEN] Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.16.00501 Plant Physiology Ò , October 2016, Vol. 172, pp. 1273–1292, www.plantphysiol.org Ó 2016 American Society of Plant Biologists. All Rights Reserved. 1273