Genome-wide analysis of OVATE family proteins in cucumber (Cucumis sativus L.)
HAN Li-jie1, SONG Xiao-fei2, WANG Zhong-yi1, LIU Xiao-feng1, YAN Li-ying3, HAN De-guo4, ZHOU Zhao-yang1, ZHANG Xiao-lan1
1 State Key Laboratories of Agrobiotechnology/Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops/MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding/China Agricultural University, Beijing 100193, P.R.China 2 Analysis and Testing Centre, Hebei Normal University of Science & Technology, Qinhuangdao 066004, P.R.China 3 College of Horticulture Science and Technology, Hebei Normal University of Science & Technology, Qinhuangdao 066004, P.R.China 4 Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of Northeast Region, Ministry of Agriculture and Rural Affairs/College of Horticulture & Landscape Architecture, Northeast Agricultural University, Harbin 150030, P.R.China
Abstract OVATE family proteins (OFPs) are plant-specific proteins with a conserved OVATE domain that regulate plant growth and development. Although OFPs have been studied in several species, their biological functions remain largely unknown in cucumber (Cucumis sativus L.). This study identified 19 CsOFPs distributed on seven chromosomes in cucumber. Most CsOFP genes were expressed in reproductive organs, but with different expression patterns. Ectopic expression of CsOFP12-16c in Arabidopsis resulted in shorter and blunt siliques. The overall results indicated that CsOFP12-16c regulates silique development in Arabidopsis and may have a similar function in cucumber.
Fund: This study was supported by the National Natural Science Foundation of China (31772315 and 31572132), and the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects, China (CEFF-PXM2019_014207_000032).
About author: HAN Li-jie, E-mail: hanlijie@cau.edu.cn; Correspondence HAN De-guo, Tel/Fax: +86-451-55190781, E-mail: deguohan@neau.edu.cn; ZHOU Zhao-yang, Tel/Fax: +86-10-62732102, E-mail: zyzhou@cau.edu.cn
HAN Li-jie, SONG Xiao-fei, WANG Zhong-yi, LIU Xiao-feng, YAN Li-ying, HAN De-guo, ZHOU Zhao-yang, ZHANG Xiao-lan.
2022.
Genome-wide analysis of OVATE family proteins in cucumber (Cucumis sativus L.). Journal of Integrative Agriculture, 21(5): 1321-1331.
Che G, Zhang X L. 2019. Molecular basis of cucumber fruit domestication. Current Opinion in Plant Biology, 47, 38–46.
Clough S J, Bent A F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Jounral, 16, 735–743.
Hackbusch J, Richter K, Muller J, Salamini F, Uhrig J F. 2005. A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proceedings of the National Academy of Sciences of the United States of America. 102, 4908–4912.
Hedrick U P, Booth N O. 1907. Mendelian characters in tomato. Proceedings of the National Academy of Sciences of the United States of America, 5, 19–24.
Huang S W, Li R Q, Zhang Z H, Li L, Gu X F, Fan W, Lucas W J, Wang X W, Xie B Y, Ni P X, Ren Y Y, Zhu H M, Li J, Lin K, Jin W W, Fei Z J, Li G C, Staub J, Kilian A, van der Vossen, et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics, 41, 1275–1281.
Huang Z J, Van Houten J, Gonzalez G, Xiao H, van der Knaap E. 2013. Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Molecular Genetics and Genomics, 288, 111–129.
Jefferson R A, Kavanagh T A, Bevan M W. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal, 6, 3901–3907.
Lazzaro M D, Wu S, Snouffer A, Wang Y P, van der Knaap E. 2018. Plant organ shapes are regulated by protein interactions and associations with microtubules. Frontiers in Plant Science, 9, 1766.
Lease K A, Wen J Q, Li J, Doke J T, Liscum E, Walke J C. 2001. A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. The Plant Cell, 13, 2631–2642.
Liu D, Sun W, Yuan Y W, Zhang N, Hayward A, Liu Y L, Wang Y. 2014. Phylogenetic analyses provide the first insights into the evolution of OVATE family proteins in land plants. Annals of Botany, 113, 1219–1233.
Liu J H, Zhang J, Hu W, Miao H X, Zhang J B, Jia C H, Wang Z, Xu B Y, Jin Z Q. 2015. Banana ovate family protein MaOFP1 and MADS-box protein MuMADS1 antagonistically regulated banana fruit ripening. PLoS ONE, 10, e0123870.
Liu J P, Van Eck J, Cong B, Tanksley S D. 2002. A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proceedings of the National Academy of Sciences of the United States of America, 99, 13302–13306.
Liu Y Y, Douglas C J. 2015. A role for OVATE FAMILY PROTEIN1 (OFP1) and OFP4 in a BLH6-KNAT7 multi-protein complex regulating secondary cell wall formation in Arabidopsis thaliana. Plant Signaling & Behavior, 10, e1033126.
Ma Y M, Yang C, He Y, Tian Z H, Li J X. 2017. Rice OVATE family protein 6 regulates plant development and confers resistance to drought and cold stresses. Journal of Experimental Botany, 68, 4885–4898.
Pagnussat G C, Yu H J, Sundaresan V. 2007. Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. The Plant Cell, 19, 3578–3592.
Pan Y P, Wang Y H, McGregor C, Liu S, Luan F S, Gao M L, Weng Y Q. 2020. Genetic architecture of fruit size and shape variation in cucurbits: A comparative perspective. Theoretical and Applied Genetics, 133, 1–21.
Price H C, Drinkard A W. 1908. Inheritance in tomato hybrids. Zeitschrift für induktive Abstammungs- und Vererbungslehre, 1, 402–403.
Rodriguez G R, Munos S, Anderson S, Sim S C, Michel A, Causse M, Gardener B B M, Francis D, van der Knaap E. 2011. Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiology, 156, 275–285.
Rogozin I B, Carmel L, Csuros M, Koonin E V. 2012. Origin and evolution of spliceosomal introns. Biology Direct, 7, 11.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Snouffer A, Kraus C, van der Knaap E. 2020. The shape of things to come: ovate family proteins regulate plant organ shape. Current Opinion in Plant Biology, 53, 98–105.
Sohlberg J J, Myrenas M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E. 2006. STY1 regulates auxin homeostasis and affects apical–basal patterning of the Arabidopsis gynoecium. The Plant Journal, 47, 112–123.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
Torii K U, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier R F, Komeda Y. 1996. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. The Plant Cell, 8, 735–746.
Trigueros M, Navarrete-Gomez M, Sato S, Christensen S K, Pelaz S, Weigel D, Yanofsky M F, Ferrandiz C. 2009. The NGATHA genes direct style development in the Arabidopsis gynoecium. The Plant Cell, 21, 1394–1409.
Tsaballa A, Pasentsis K, Darzentas N, Tsaftaris A S. 2011. Multiple evidence for the role of an Ovate-like gene in determining fruit shape in pepper. BMC Plant Biology, 11, 46.
Wang S C, Chang Y, Ellis B. 2016. Overview of OVATE FAMILY PROTEINS, a novel class of plant-specific growth regulators. Frontiers in Plant Science, 7, 417.
Wang S C, Chang Y, Guo J J, Chen J G. 2007. Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation. The Plant Journal, 50, 858–872.
Wang S C, Chang Y, Guo J J, Zeng Q N, Ellis B E, Chen J G. 2011. Arabidopsis Ovate Family Proteins, a novel transcriptional repressor family, control multiple aspects of plant growth and development. PLoS ONE, 6, e23896.
Wang Y K, Chang W C, Liu P F, Hsiao M K, Lin C T, Lin S M, Pan R L. 2010. Ovate family protein 1 as a plant Ku70 interacting protein involving in DNA double-strand break repair. Plant Molecular Biology. 74, 453–466.
Wang Y P, Wang Q B, Hao W, Sun H H, Zhang L. 2020. Characterization of the OFP gene family and its putative involvement of tuberous root shape in radish. International Journal of Molecular Sciences, 21, 1293.
Weng Y Q, Colle M, Wang Y H, Yang L M, Rubinstein M, Sherman A, Ophir R, Grumet R. 2015. QTL mapping in multiple populations and development stages reveals dynamic quantitative trait loci for fruit size in cucumbers of different market classes. Theoretical and Applied Genetics, 128, 1747–1763.
Wu S, Zhang B Y, Keyhaninejad N, Rodríguez G R, Kim H J, Chakrabarti M, Illa-Berenguer E, Taitano N K, Gonzalo M J, Díaz A, Pan Y P, Leisner C P, Halterman D, Buell C R, Weng Y Q, Jansky S H, van Eck H, Willemsen J, Monforte A J, Meulia T, et al. 2018. A common genetic mechanism underlies morphological diversity in fruits and other plant organs. Nature Communications, 9, 4734.
Xin T X, Zhang Z, Li S, Zhang S, Li Q, Zhang Z H, Huang S W, Yang X Y. 2019. Genetic regulation of ethylene dosage for cucumber fruit elongation. The Plant Cell, 31, 1063–1076.
Yang C, Ma Y M, He Y, Tian Z H, Li J X. 2018. OsOFP19 modulates plant architecture by integrating the cell division pattern and brassinosteroid signaling. The Plant Journal, 93, 489–501.
Yang C, Shen W J, He Y, Tian Z H, Li J X. 2016. OVATE family protein 8 positively mediates brassinosteroid signaling through interacting with the GSK3-like kinase in rice. PLoS Genetics, 12, e1006118.
Yu H, Jiang W Z, Liu Q, Zhang H, Piao M X, Chen Z D, Bian M D. 2015. Expression pattern and subcellular localization of the ovate protein family in rice. PLoS ONE, 10, e0118966.
Zhang Z, Wang B W, Wang S H, Lin T, Yang L, Zhao Z L, Zhang Z H, Huang S W, Yang X Y. 2019. Genome-wide target mapping shows histone deacetylase complex 1 regulates cell proliferation in cucumber fruit. Plant Physiology, 182, 167–184.
Zhao D S, Li Q F, Zhang C Q, Zhang C, Yang Q Q, Pan L X, Ren X Y, Lu J, Gu M H, Liu Q Q. 2018. GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality. Nature Communications, 9, 1240.
Zhao J Y, Jiang L, Che G, Pan Y P, Li Y Q, Hou Y, Zhao W S, Zhong Y T, Ding L, Yan S S, Sun C Z, Liu R Y, Yan L Y, Wu T, Li X X, Weng Y Q, Zhang X L. 2019. A functional allele of CsFUL1 regulates fruit length through inhibiting CsSUP and auxin transport in cucumber. The Plant Cell, 31, 1289–1307.
Zhou H, Ma R J, Gao L, Zhang J Y, Zhang A D, Zhang X J, Ren F, Zhang W H, Liao L, Yang Q R, Xu S L, Ogutu C O, Zhao J B, Yu M L, Jiang Q, Korban S S, Han Y P. 2020. A 1.7-Mb chromosomal inversion downstream of a PpOFP1 gene is responsible for flat fruit shape in peach. Plant Biotechnology Journal, 19, 192–205.
WANG Jie, LI Shuai, CHEN Chen, ZHANG Qi-qi, ZHANG Hui-min, CUI Qing-zhi, CAI Guang-hua, ZHANG Xiao-peng, CHAI Sen, WAN Li, YANG Xue-yong, ZHANG Zhong-hua, HUANG San-wen, CHEN Hui-ming, SUN Jin-jing. A novel mutation in ACS11 leads to androecy in cucumber[J]. >Journal of Integrative Agriculture, 2023, 22(11): 3312-3320.
CHEN Chen, CUI Qing-zhi, HUANG San-wen, WANG Shen-hao, LIU Xiao-hong, LU Xiang-yang, CHEN Hui-ming, TIAN Yun. An EMS mutant library for cucumber[J]. >Journal of Integrative Agriculture, 2018, 17(07): 1612-1619.
