Phylogenetic and Expression Analysis of MADS-box Gene Family in Rhododendron ovatum

doi:10.11983/CBB22105

Abstract

Abstract: Rhododendron is famous for its diversity and ornamental value. Rhododendron ovatum has unique flower type and low-altitude adaptability, thus possessing landscape application prospect in southern China. In this study, we analyzed evolutionary pattern within Ericales based on recently published genomes, and identified key genes underlying flower development of R. ovatum. Phylogenetic analysis showed that the number of MADS-box genes in three representative species of Rhododendron (R. ovatum, R. simsii, and R. delavayi) was relatively consistent and can be divided into 19 subfamilies, including AP1, AP3, PI, AG, and SEP. MADS-box gene have expanded, especially SVP, ANR1, Mα, Mβ, and Mγ. Multiple copies were retained in AG and SEP clades in R. ovatum. While a few copies of AP3/PI gene, indicating a more conservative evolutionary pattern. The transcriptome data illustrated tissue-specific expression pattern in MADS-box genes, among which AP1, AP3/PI, AG, SEP and MIKC* genes are specifically expressed in floral organs. Overall, we discussed evolutionary history of MADS-box gene family in R. ovatum and proposed functions, providing reference for further study the flower development and functional analysis of MADS-box genes in R. ovatum.

Key words: Rhododendron ovatum, Ericaceae, MADS-box gene family, flower development, expression analysis

Fuhui Sun, Huiyi Fang, Xiaohui Wen, Liangsheng Zhang. Phylogenetic and Expression Analysis of MADS-box Gene Family in Rhododendron ovatum[J]. Chinese Bulletin of Botany, 2023, 58(3): 404-416.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB22105

https://www.chinbullbotany.com/EN/Y2023/V58/I3/404

Figures/Tables 7

Figure 1 The phylogenetic tree and MADS-box gene numbers of Rhododendron ovatum and nine other species in the context of angiosperms

Figure 2 Maximum likelihood phylogenetic tree constructed by Rhododendron ovatum, Arabidopsis thaliana and Vitis vinifera MADS-box genes R. ovatum homologous genes are in red font.

Figure 3 Maximum likelihood phylogenetic trees of floral identity genes (A) Phylogenetic tree of AP1/FUL genes; (B) Phylogenetic tree of AP3/PI genes; (C) Phylogenetic tree of AG genes; (D) Phylogenetic tree of SEP genes. Rhododendron ovatum homologous genes are in red font.

Figure 4 Analysis of structure of Rhododendron ovatum MADS-box protein (A) Phylogenetic tree of R. ovatum MADS-box genes; (B) Conserved motif analysis; (C) Conserved domain analysis

Figure 5 Structures of Rhododendron ovaturn MADS-box proteins’ conserved domain (A) MADS MEF2-like domain; (B) K-box domain; (C) MADS SRF-like domain

Figure 6 Chromosomal localization and collinearity analysis of Rhododendron ovatum MADS-box genes The tracks from outer to inner circles represent the gene location on chromosomes, gene density, and collinear regions (red lines indicate MADS-box genes).

Figure 7 Expression analysis of Rhododendron ovatum MADS-box genes (A) Expression analysis of R. ovatum MADS-box genes in different tissues (the floral identity genes are in red); (B) Proposed ABCE flower development model of R. ovatum (the bar height represents the expression level)

References 33

[1]	丁献华, 陈伟, 张直峰 (2020). 荷花B类MADS-box基因家族NnDEF基因的克隆及表达分析. 上海农业学报 36, 1-7.
[2]	高虎虎, 张云霄, 胡胜武, 郭媛 (2017). 甘蓝型油菜MADS- box基因家族的鉴定与系统进化分析. 植物学报 52, 699-712. DOI
[3]	高玮林, 张力曼, 薛超玲, 张垚, 刘孟军, 赵锦 (2022). 枣E类MADS基因在花和果中的表达及其蛋白互作研究. 园艺学报 49, 739-748. DOI
[4]	耿兴敏, 宦智群, 苏家乐, 刘晓青 (2021). 杜鹃花属植物种质创新研究进展. 分子植物育种 19, 604-613.
[5]	景丹龙, 郭启高, 陈薇薇, 夏燕, 吴頔, 党江波, 何桥, 梁国鲁 (2018). 被子植物花器官发育的模型演变和分子调控. 植物生理学报 54, 355-362.
[6]	景丹龙, 夏燕, 张守攻, 王军辉 (2016). 黄金树B类MADS- box基因表达特征分析. 植物学报 51, 210-217. DOI
[7]	王莹, 穆艳霞, 王锦 (2021). MADS-box基因家族调控植物花器官发育研究进展. 浙江农业学报 33, 1149-1158. DOI
[8]	徐启江, 关录飞, 吴笑女, 孙丽, 谭文勃, 聂玉哲, 李玉花 (2008). 草原龙胆MADS-box基因的克隆及表达分析. 植物学通报 25, 415-429.
[9]	杨华, 宋绪忠 (2016). 高温胁迫对马银花的生理指标影响. 林业科技通讯 01, 3-6.
[10]	杨丽, 严露露, 李慧娥, 杜致辉, 郑淇元 (2021). 映山红杜鹃MADS基因家族的鉴定与分析. 分子植物育种 19, 6290-6301.
[11]	Airoldi CA, Davies B (2012). Gene duplication and the evolution of plant MADS-box transcription factors. J Genet Genomics 39, 157-165. DOI PMID
[12]	Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, De Pouplana LR, Martínez-Castilla L, Yanofsky MF (2000). An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA 97, 5328-5333. PMID
[13]	Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020). TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13, 1194-1202. DOI PMID
[14]	Chen F, Zhang XT, Liu X, Zhang LS (2017). Evolutionary analysis of MIKC^C-type MADS-box genes in gymnosperms and angiosperms. Front Plant Sci 8, 895. DOI PMID
[15]	Duarte JM, Cui LY, Wall PK, Zhang Q, Zhang XH, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006). Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23, 469-478. PMID
[16]	Edgar RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797. DOI PMID
[17]	Lee JH, Ryu HS, Chung KS, Posé D, Kim S, Schmid M, Ahn JH (2013). Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342, 628-632. DOI PMID
[18]	Litt A, Kramer EM (2010). The ABC model and the diversification of floral organ identity. Semin Cell Dev Biol 21, 129-137. DOI PMID
[19]	Liu Y, Cui SJ, Wu F, Yan S, Lin XL, Du XQ, Chong K, Schilling S, Theißen G, Meng Z (2013). Functional conservation of MIKC-type MADS box genes in Arabidopsis* and rice pollen maturation. Plant Cell 25, 1288-1303. DOI URL
[20]	Pařenicová L, De Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15, 1538-1551. DOI URL
[21]	Price MN, Dehal PS, Arkin AP (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26, 1641-1650. DOI PMID
[22]	Qiu YC, Köhler C (2022). Endosperm evolution by duplicated and neofunctionalized Type I MADS-box transcription factors. Mol Biol Evol 39, msab355.
[23]	Ruelens P, Zhang ZC, Van Mourik H, Maere S, Kaufmann K, Geuten K (2017). The origin of floral organ identity quartets. Plant Cell 29, 229-242. DOI URL
[24]	Shan HY, Cheng J, Zhang R, Yao X, Kong HZ (2019). Developmental mechanisms involved in the diversification of flowers. Nat Plants 5, 917-923. DOI PMID
[25]	Smaczniak C, Immink RGH, Angenent GC, Kaufmann K (2012). Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139, 3081-3098. DOI PMID
[26]	Theißen G, Kim JT, Saedler H (1996). Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43, 484-516. PMID
[27]	Theißen G, Melzer R, Rümpler F (2016). MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143, 3259-3271. DOI PMID
[28]	Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, Maere S, Van De Peer Y, Geuten K (2012). Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol Biol Evol 29, 3793-3806. DOI PMID
[29]	Wang XY, Gao Y, Wu XP, Wen XH, Li DQ, Zhou H, Li Z, Liu B, Wei JF, Chen F, Chen F, Zhang CJ, Zhang LS, Xia YP (2021). High-quality evergreen azalea genome reveals tandem duplication-facilitated low-altitude adaptability and floral scent evolution. Plant Biotechnol J 19, 2544-2560. DOI PMID
[30]	Wen XH, Li JZ, Wang LL, Lu CF, Gao Q, Xu P, Pu Y, Zhang QL, Hong Y, Hong L, Huang H, Xin HG, Wu XY, Kang DR, Gao K, Li YJ, Ma CF, Li XM, Zheng HK, Wang ZC, Jiao YN, Zhang LS, Dai SL (2022). The Chrysanthemum lavandulifolium genome and the molecular mechanism underlying diverse capitulum types. Hortic Res 9, uhab022.
[31]	Wu WW, Huang XT, Cheng J, Li ZG, De Folter S, Huang ZR, Jiang XQ, Pang HX, Tao SH (2011). Conservation and evolution in and among SRF- and MEF2-type MADS domains and their binding sites. Mol Biol Evol 28, 501-511. DOI PMID
[32]	Yang FS, Nie S, Liu H, Shi TL, Tian XC, Zhou SS, Bao YT, Jia KH, Guo JF, Zhao W, An N, Zhang RG, Yun QZ, Wang XZ, Mannapperuma C, Porth I, El-Kassaby YA, Street NR, Wang XR, Van De Peer Y, Mao JF (2020). Chromosome-level genome assembly of a parent species of widely cultivated azaleas. Nat Commun 11, 5269. DOI
[33]	Zhang LS, Chen F, Zhang XT, Li Z, Zhao YY, Lohaus R, Chang XJ, Dong W, Ho SYW, Liu X, Song AX, Chen JH, Guo WL, Wang ZJ, Zhuang YY, Wang HF, Chen XQ, Hu J, Liu YH, Qin Y, Wang K, Dong SS, Liu Y, Zhang SZ, Yu XX, Wu Q, Wang LS, Yan XQ, Jiao YN, Kong HZ, Zhou XF, Yu CW, Chen YC, Li F, Wang JH, Chen W, Chen XL, Jia QD, Zhang C, Jiang YF, Zhang WB, Liu GH, Fu JY, Chen F, Ma H, Van De Peer Y, Tang HB (2020). The water lily genome and the early evolution of flowering plants. Nature 577, 79-84. DOI