辣椒中 CaYABBY 家族的全基因组分析以及 CaYABBY5 在花决定性和果实形态调控中的功能鉴定

doi:10.1016/j.jia.2025.03.025

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (8): 3024-3039.DOI: 10.1016/j.jia.2025.03.025

辣椒中 CaYABBY 家族的全基因组分析以及 CaYABBY5 在花决定性和果实形态调控中的功能鉴定

收稿日期:2024-10-24 修回日期:2025-03-27 接受日期:2025-03-11 出版日期:2025-07-20 发布日期:2025-07-16

Genome-wide analysis of the CaYABBY family in pepper and functional identification of CaYABBY5 in the regulation of floral determinacy and fruit morphogenesis

Ke Fang^{1, 2}, Yi Liu^{1, 2}, Zhiquan Wang^{1, 2}, Xiang Zhang^{1, 2}, Xuexiao Zou^{1, 2}, Feng Liu^{1, 2#}, Zhongyi Wang^{1, 2#}

¹Engineering Research Center for Horticultural Crop Germplasm Creation and New Variety Breeding/Key Laboratory of Vegetable Biology of Hunan Province, College of Horticulture, Hunan Agricultural University, Changsha 410128, China
²Yuelushan Laboratory, Changsha 410128, China

Received:2024-10-24 Revised:2025-03-27 Accepted:2025-03-11 Online:2025-07-20 Published:2025-07-16
About author:Ke Fang, E-mail: fk.wz@stu.hunau.edu.cn; #Correspondence Zhongyi Wang, E-mail: wangzhy@hunau.edu.cn; Feng Liu, E-mail: jwszjx@hunau.edu.cn
Supported by:
This work was financially supported by the National Key Research and Development Program of China (2023YFD2300702), the Science and Technology Innovation Program of Hunan Province, China (2024RC3189), and the Natural Science Foundation of Hunan Province, China (2024JJ4023).

摘要/Abstract

摘要：

辣椒果实因其辛辣的口感、多样的风味和较高的营养价值而备受青睐。花器官和果实的发育直接决定了辣椒果实的品质。YABBY 基因家族在植物生长发育过程中发挥着多种重要功能，对花器官的发育具有至关重要的作用，但其在辣椒中的具体功能尚不明确。本研究系统鉴定了辣椒基因组中9个CaYABBY基因，发现其成员在生殖器官中呈现差异表达特征。其中，特异性表达于花瓣和心皮的CaYABBY5基因，通过辣椒基因沉默和番茄异位表达双重验证，揭示了该基因通过调控心皮形态发生影响花器官决定性与果实形态建成。蛋白互作分析发现，CaYABBY5与SEPALLATA3同源蛋白（SEP3）存在相互作用，且两者在辣椒花器官中呈现高度一致的表达模式，表明二者可能通过协同作用调控花-果形态建成。该研究首次解析了辣椒YABBY基因家族的功能特征，为茄科作物花器官发育调控网络研究提供了新视角。

Abstract:

Pepper fruit is highly favored for its spicy taste, diverse flavors, and significant nutritional benefits. The proper development of flowers and fruits directly determines the quality of pepper fruit. The YABBY gene family exhibits diverse functions in growth and development, which is crucial to the identity of flower organs. However, the specific functions of these genes in pepper remain unclear. In this study, nine CaYABBY genes were identified and characterized in pepper. Most CaYABBY genes were highly expressed in reproductive organs, albeit with varying expression patterns. The CaYABBY5 gene, uniquely expressed in petals and carpels, has been demonstrated to modulate floral organ determinacy and fruit shape through gene silencing in pepper and ectopic expression in tomato. Protein interaction analysis revealed an interacting protein SEPALLATA3-like protein (SEP3), exhibiting a similar expression profile to CaYABBY5. These findings suggest that CaYABBY5 may modulate the morphogenesis of floral organs and fruits by interacting with CaSEP3. This study provided valuable insights into the classification and function of CaYABBY genes in pepper.

Key words: YABBY transcription factor , pepper , expression pattern , CaYABBY5 , CaSEP3 , flower organs development

Ke Fang, Yi Liu, Zhiquan Wang, Xiang Zhang, Xuexiao Zou, Feng Liu, Zhongyi Wang. 辣椒中 CaYABBY 家族的全基因组分析以及 CaYABBY5 在花决定性和果实形态调控中的功能鉴定[J]. Journal of Integrative Agriculture, 2025, 24(8): 3024-3039.

Ke Fang, Yi Liu, Zhiquan Wang, Xiang Zhang, Xuexiao Zou, Feng Liu, Zhongyi Wang. Genome-wide analysis of the CaYABBY family in pepper and functional identification of CaYABBY5 in the regulation of floral determinacy and fruit morphogenesis[J]. Journal of Integrative Agriculture, 2025, 24(8): 3024-3039.

参考文献

Adal A M, Binson E, Remedios L, Mahmoud S S. 2021. Expression of lavender AGAMOUS-like and SEPALLATA3-like genes promote early flowering and alter leaf morphology in Arabidopsis thaliana. Planta, 254, 54.

Alvarez J, Smyth D R. 1999. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development, 126, 2377–2386.

Bailey T L, Johnson J, Grant C E, Noble W S. 2015. The MEME suite. Nucleic Acids Research, 43, 39–49.

Borovsky Y, Raz A, Doron-Faigenboim A, Zemach H, Karavani E, Paran I. 2022. Pepper fruit elongation is controlled by Capsicum annuum ovate family protein 20. Frontiers in Plant Science, 12, 815589.

Bowman J L. 2000. The YABBY gene family and abaxial cell fate. Current Opinion in Plant Biology, 3, 17–22.

Bowman J L, Smyth D R. 1999. CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development, 126, 2387–2396.

Castañeda L, Giménez E, Pineda B, García-Sogo B, Ortiz-Atienza A, Micol-Ponce R, Angosto T, Capel J, Moreno V, Yuste-Lisbona F J, Lozano R. 2022. Tomato CRABS CLAW paralogues interact with chromatin remodeling factors to mediate carpel development and floral determinacy. New Phytologist, 234, 1059–1074.

Che G, Pan Y, Liu X, Li M, Zhao J, Yan S, He Y, Wang Z, Cheng Z, Song W, Zhou Z, Wu T, Weng Y, Zhang X. 2023a. Natural variation in CRABS CLAW contributes to fruit length divergence in cucumber. The Plant Cell, 35, 738–755.

Che G, Song W, Zhang X. 2023b. Gene network associates with CsCRC regulating fruit elongation in cucumber. Vegetable Research, 3, 7.

Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.

Dai M, Zhao Y, Ma Q, Hu Y, Hedden P, Zhang Q, Zhou D X. 2007. The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiology, 144, 121–133.

Ding B, Li J, Gurung V, Lin Q, Sun X, Yuan Y. 2021. The leaf polarity factors SGS3 and YABBYs regulate style elongation through auxin signaling in Mimulus lewisii. New Phytologist, 232, 2191–2206.

Fernandez-Pozo N, Menda N, Edwards J D, Saha S, Tecle I Y, Strickler S R, Bombarely A, Fisher-York T, Pujar A, Foerster H, Yan A, Mueller L A. 2015. The Sol Genomics Network (SGN) - from genotype to phenotype to breeding. Nucleic Acids Research, 43, 1036–1041.

Gasteiger E. 2003. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research, 31, 3784–3788.

Goldshmidt A, Alvarez J P, Bowman J L, Eshed Y. 2008. Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems. The Plant Cell, 20, 1217–1230.

Hao L, Zhang J, Shi S, Li P, Li D, Zhang T, Guo H. 2022. Identification and expression profiles of the YABBY transcription factors in wheat. PeerJ, 10, 12855.

He Q, Wu H, Zeng L, Yin C, Wang L, Tan Y, Lv W, Liao Z, Zheng X, Zhang S, Han Q, Wang D, Zhang Y, Xiong G, Wang Q. 2024. OsKANADI1 and OsYABBY5 regulate rice plant height by targeting GIBERELLIN 2-OXIDASE6. The Plant Cell, 37, koae276.

Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409, 525–529.

Huang F, Xu G, Chi Y, Liu H, Xue Q, Zhao T, Gai J, Yu D. 2014. A soybean MADS-box protein modulates floral organ numbers, petal identity and sterility. BMC Plant Biology, 14, 89.

Kong L, Sun J, Jiang Z, Ren W, Wang Z, Zhang M, Liu X, Wang L, Ma W, Xu J. 2023. Identification and expression analysis of YABBY family genes in Platycodon grandiflorus. Plant Signaling & Behavior, 18, 2163069.

Lamesch P, Berardini T Z, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander D L, Garcia-Hernandez M, Karthikeyan A S, Lee C H, Nelson W D, Ploetz L, Singh S, Wensel A, Huala E. 2012. The Arabidopsis Information Resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Research, 40, 1202–1210.

Lescot M. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.

Letunic I, Khedkar S, Bork P. 2021. SMART: Recent updates, new developments and status in 2020. Nucleic Acids Research, 49, 458–460.

Li T, Zhang M, Li M, Wang X, Xing S. 2023. Molecular characterization and expression analysis of YABBY genes in Chenopodium quinoa. Genes, 14, 2103.

Li Z, Li G, Cai M, Priyadarshani S V G N, Aslam M, Zhou Q, Huang X, Wang X, Liu Y, Qin Y. 2019. Genome-wide analysis of the YABBY transcription factor family in pineapple and functional identification of AcYABBY4 involvement in salt stress. International Journal of Molecular Sciences, 20, 5863.

Lin Z Y, Zhu G F, Lu C Q, Gao J, Li J, Xie Q, Wei Y L, Jin J P, Wang F L, Yang F X. 2023. Functional conservation and divergence of SEPALLATA-like genes in floral development in Cymbidium sinense. Frontiers in Plant Science, 14, 1209834.

Liu F, Yu H, Deng Y, Zheng J, Liu M, Ou L, Yang B, Dai X, Ma Y, Feng S, He S, Li X, Zhang Z, Chen W, Zhou S, Chen R, Liu M, Yang S, Wei R, Li H, et al. 2017. PepperHub, an informatics hub for the chili pepper research community. Molecular Plant, 10, 1129–1132.

Liu F, Zhao J, Sun H, Xiong C, Sun X, Wang X, Wang Z, Jarret R, Wang J, Tang B, Xu H, Hu B, Suo H, Yang B, Ou L, Li X, Zhou S, Yang S, Liu Z, Yuan F, et al. 2023. Genomes of cultivated and wild Capsicum species provide insights into pepper domestication and population differentiation. Nature Communication, 14, 5487.

Liu G, Li C, Yu H, Tao P, Yuan L, Ye J, Chen W, Wang Y, Ge P, Zhang J, Zhou G, Zheng W, Ye Z, Zhang Y. 2020. GREEN STRIPE, encoding methylated TOMATO AGAMOUS-LIKE 1, regulates chloroplast development and Chl synthesis in fruit. New Phytologist, 228, 302–317.

Lu S, Wang J, Chitsaz F, Derbyshire M K, Geer R C, Gonzales N R, Gwadz M, Hurwitz D I, Marchler G H, Song J S, Thanki N, Yamashita R A, Yang M, Zhang D, Zheng C, Lanczycki C J, Marchler-Bauer A. 2020. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Research, 48, 265–268.

Lu Y, Zhu H. 2022. The regulation of nutrient and flavor metabolism in tomato fruit. Vegetable Research, 2, 5.

Masiero S, Colombo L, Grini P E, Schnittger A, Kater M M. 2011. The emerging importance of type I MADS box transcription factors for plant reproduction. The Plant Cell, 23, 865–872.

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar G A, Sonnhammer E L L, Tosatto S C E, Paladin L, Raj S, Richardson L J, Finn R D, Bateman A. 2021. Pfam: The protein families database in 2021. Nucleic Acids Research, 49, 412–419.

Pelaz S, Ditta G S, Baumann E, Wisman E, Yanofsky M F. 2000. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 405, 200–203.

Pelaz S, Gustafson-Brown C, Kohalmi S E, Crosby W L, Yanofsky M F. 2001. APETALA1 and SEPALLATA3 interact to promote flower development. The Plant Journal, 26, 385–394.

Robles P, Pelaz S. 2005. Flower and fruit development in Arabidopsis thaliana. International Journal of Developmental Biology, 49, 633–643.

Sakai H, Lee S S, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang C, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T. 2013. Rice annotation project database (RAP-DB): An Integrative and interactive database for rice genomics. Plant and Cell Physiology, 54, 6.

Sarojam R, Sappl P G, Goldshmidt A, Efroni I, Floyd S K, Eshed Y, Bowman J L. 2010. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. The Plant Cell, 22, 2113–2130.

Sawa S, Watanabe K, Goto K, Kanaya E, Morita E H, Okada K. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes & Development, 13, 1079–1088.

Shen H, Luo B, Ding Y, Xiao H, Chen G, Yang Z, Hu Z, Wu T. 2024. The YABBY transcription factor, SlYABBY2a, positively regulates fruit septum development and ripening in tomatoes. International Journal of Molecular Sciences, 25, 5206.

Siegfried K R, Eshed Y, Baum S F, Otsuga D, Drews G N, Bowman J L. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development, 126, 4117–4128.

Smaczniak C, Immink R G, Muiño J M, Blanvillain R, Busscher M, Busscher-Lange J, Dinh Q D, Liu S, Westphal A H, Boeren S, Parcy F, Xu L, Carles C C, Angenent G C, Kaufmann K. 2012a. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences of the United States of America, 109, 1560–1565.

Smaczniak C, Immink R G H, Angenent G C, Kaufmann K. 2012b. Developmental and evolutionary diversity of plant MADS-domain factors: Insights from recent studies. Development, 139, 3081–3098.

Song J, Shang L, Li C, Wang W, Wang X, Zhang C, Ai G, Ye J, Yang C, Li H, Hong Z, Larkin RM, Ye Z, Zhang J. 2022. Variation in the fruit development gene POINTED TIP regulates protuberance of tomato fruit tip. Nature Communication, 13, 5940.

Sun L, Wei Y Q, Wu K H, Yan J Y, Xu J N, Wu Y R, Li G X, Xu J M, Harberd N P, Ding Z J, Zheng S J. 2021. Restriction of iron loading into developing seeds by a YABBY transcription factor safeguards successful reproduction in Arabidopsis. Molecular Plant, 14, 1624–1639.

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.

Villanueva J M, Broadhvest J, Hauser B A, Meister R J, Schneitz K, Gasser C S. 1999. INNER NO OUTER regulates abaxial-adaxial patterning in Arabidopsis ovules. Genes & Development, 13, 3160–3169.

Vrebalov J, Pan I L, Arroyo A J M, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, Irish V F. 2009. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. The Plant Cell, 21, 3041–3062.

Wan H, Yuan W, Ruan M, Ye Q, Wang R, Li Z, Zhou G, Yao Z, Zhao J, Liu S, Yang Y. 2011. Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.). Biochemical and Biophysical Research Communications, 416, 24–30.

Wang Q, Reddy V A, Panicker D, Mao H, Kumar N, Rajan C, Venkatesh P N, Chua N, Sarojam R. 2016. Metabolic engineering of terpene biosynthesis in plants using a trichome-specific transcription factor MsYABBY5 from spearmint (Mentha spicata). Plant Biotechnology Journal, 14, 1619–1632.

Wang S, Wang K, Li Z, Li Y, He J, Li H, Wang B, Xin T, Tian H, Tian J, Zhang G, Li H, Huang S, Yang X. 2022. Architecture design of cucurbit crops for enhanced productivity by a natural allele. Nature Plants, 8, 1394–1407.

Wang W, Ma J, Liu H, Wang Z, Nan R, Zhong T, Sun M, Wang S, Yao Y, Sun F, Zhang C, Xi Y. 2024. Genome-wide analysis of the switchgrass YABBY family and functional characterization of PvYABBY14 in response to ABA and GA stress in Arabidopsis. BMC Plant Biology, 24, 114.

Weigel D, Meyerowitz E M. 1994. The ABCs of floral homeotic genes. Cell, 78, 203–209.

Wheeler T J, Eddy S R. 2013. nhmmer: DNA homology search with profile HMMs. Bioinformatics, 29, 2487–2489.

Wu J, Li P, Li M, Zhu D, Ma H, Xu H, Li S, Wei J, Bian X, Wang M, Lai Y, Peng Y, Li H, Rahman A, Wu S. 2024a. Heat stress impairs floral meristem termination and fruit development by affecting the BR-SlCRCa cascade in tomato. Plant Communications, 5,100790.

Wu J, Li P, Zhu D, Ma H, Li M, Lai Y, Peng Y, Li H, Li S, Wei J, Bian X, Rahman A, Wu S. 2024b. SlCRCa is a key D-class gene controlling ovule fate determination in tomato. Plant Biotechnology Journal, 22, 1966–1980.

Xiang L, Chen Y, Chen L, Fu X, Zhao K, Zhang J, Sun C. 2018. B and E MADS-box genes determine the perianth formation in Cymbidium goeringii Rchb.f. Physiologia Plantarum, 162, 353–369.

Yan S, Ning K, Wang Z, Liu X, Zhong Y, Ding L, Zi H, Cheng Z, Li X, Shan H, Lv Q, Luo L, Liu R, Yan L, Zhou Z, Lucas W J, Zhang X. 2020. CsIVP functions in vasculature development and downy mildew resistance in cucumber. PLoS Biology, 18, 3000671.

Yang T, He Y, Niu S, Zhang Y. 2022. A YABBY gene CRABS CLAW a (CRCa) negatively regulates flower and fruit sizes in tomato. Plant Science, 320, 111285.

Yu Y, Hu H, Voytas D F, Doust A N, Kellogg E A. 2023. The YABBY gene SHATTERING1 controls activation rather than patterning of the abscission zone in Setaria viridis. New Phytologist, 240, 846–862.

Zhang S, Tan F Q, Chung C H, Slavkovic F, Devani R S, Troadec C, Marcel F, Morin H, Camps C, Gomez Roldan M V, Benhamed M, Dogimont C, Boualem A, Bendahmane A. 2022. The control of carpel determinacy pathway leads to sex determination in cucurbits. Science, 378, 543–549.

Zhang T, Wu A, Hu X, Deng Q, Ma Z, Su L. 2023. Comprehensive study of rice YABBY gene family: evolution, expression and interacting proteins analysis. PeerJ, 11, 14783.

Zhang X, Ding L, Song A, Li S, Liu J, Zhao W, Jia D, Guan Y, Zhao K, Chen S, Jiang J, Chen F. 2022. DWARF AND ROBUST PLANT regulates plant height via modulating gibberellin biosynthesis in chrysanthemum. Plant Physiology, 190, 2484–2500.

Zhang Y, Zhang B, Yang T, Zhang J, Liu B, Zhan X, Liang Y. 2020. The GAMYB-like gene SlMYB33 mediates flowering and pollen development in tomato. Horticulture Research, 7, 133.

Zhao S P, Lu D, Yu T F, Ji Y J, Zheng W J, Zhang S X, Chai S C, Chen Z Y, Cui X Y. 2017. Genome-wide analysis of the YABBY family in soybean and functional identification of GmYABBY10 involvement in high salt and drought stresses. Plant Physiology and Biochemistry, 119, 132–146.

Zhao T, Ni Z, Dai Y, Yao Y, Nie X, Sun Q. 2006. Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.). Molecular Genetics and Genomics, 276, 334.

Zhou Z, Bi G, Zhou J M. 2018. Luciferase complementation assay for protein-protein interactions in plants. Current Protocols in Molecular Biology, 3, 42–50.

Zhu Q, Deng L, Chen J, Rodríguez GR, Sun C, Chang Z, Yang T, Zhai H, Jiang H, Topcu Y, Francis D, Hutton S, Sun L, Li CB, van der Knaap E, Li C. 2023. Redesigning the tomato fruit shape for mechanized production. Nature Plants, 9, 1659–1674.

辣椒中 CaYABBY 家族的全基因组分析以及 CaYABBY5 在花决定性和果实形态调控中的功能鉴定

Genome-wide analysis of the CaYABBY family in pepper and functional identification of CaYABBY5 in the regulation of floral determinacy and fruit morphogenesis

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