Evolutionary Characteristics and Functional Inferences of Core MADS-box Transcription Factors in Potato

doi:10.13560/j.cnki.biotech.bull.1985.2025-1350

Abstract

Abstract:

Objective The MADS-box transcription factor family is widely involved in plant growth, development, and floral organ formation. This study systematically analyzes the function of core MADS-box transcription factors across 51 potato genomes, aiming to provide a theoretical basis and genetic resources for molecular breeding in potato (Solanum tuberosum L.). Method Based on whole-genome data from 33 wild and 18 cultivated diploid potatoes, core MADS-box genes were identified. Bioinformatics analysis was conducted to investigate their physicochemical properties, phylogenetic relationships, chromosomal distribution, and conserved domains. Expression patterns were analyzed by integrating transcriptome data and RT-qPCR. Their biological functions were inferred through GO enrichment analysis, exogenous hormone treatment, and comparison with functionally characterized homologous genes from major crops. Collinearity analysis was also performed on closely related species. Result A total of 95 common MADS-box genes, referred to as core genes, were identified across 51 diploid potatoes, classified into two major subfamilies: Type I (Mα, Mβ, Mγ) and Type II (MIKC*, MIKCc). Physicochemical analysis indicated that these proteins are generally hydrophilic and unstable. Phylogenetic and structural analyses revealed that each subfamily possesses characteristic motifs and domains. Chromosomal mapping showed that the genes are clustered on chromosomes Chr01, Chr04, Chr05, and Chr12. Expression pattern analysis indicated that several MIKC^c-type genes are specifically expressed in floral buds, stolons, and other tissues. GO enrichment analysis demonstrated that this family is involved in floral organ development and hormone response processes. Hormone response analysis revealed that the expressions of key candidate genes are suppressed by GA₃ and induced by ABA. Phylogenetic comparison with functional genes such as OsMADS29 from rice suggested that some genes may participate in tuber development and yield formation. Collinearity analysis revealed 37 conserved MADS-box genes between potato and its close relatives, with some genes exhibiting translocation variations. Conclusion The MADS-box gene family in potatoes retains conserved functions in regulating floral and tuber development during evolution. Candidate genes such as DM8C02G24490.1 and DM8C03G29590.1, which are associated with seed development and tuber formation, provide important targets for subsequent functional validation and breeding improvement.

Key words: potato, transcription factor, MADS-box, gene family, tuber development

DONG Ya-rui, LI Jin-ye, CUI Qing-han, JIA Yu-xin. Evolutionary Characteristics and Functional Inferences of Core MADS-box Transcription Factors in Potato[J]. Biotechnology Bulletin, 2026, 42(6): 64-76.

Figures/Tables 10

Fig. 1 Distribution of MADS-box gene family in various potato germplasm resources

Fig. 2 Phylogenetic relationship of the core MADS-box in potato

Fig. 3 Characteristics of the core MADS-box genes in potato

Fig. 4 Chromosomal distribution of core MADS-box genes in potato

Fig. 5 GO enrichment analysis of core MADS-box transcription factors in potato

Fig. 6 Tissue expression patterns of core MADS-box genes in potato under different photoperiods

Fig. 7 Relative expressions of MADS-box genes under specific light conditions (A) and their expression patterns in response to GA3 and ABA treatments (A)

Fig. 8 Relative expressions of genes MADS-box during flower and tuber developmentF1: Inflorescence development stage. F2: Flower organ formation stage. F3: Flower bud maturation stage. F4: Flowering stage; F5: Fertilization and fruit-setting stage. F6: Flower abscission stage. S1: Stolon initiation stage. S2: Tuber initiation stage. S3: Tuber organ establishment stage

Fig. 9 Phylogenetic relationship of the core MADS-box genes in potato with the known functional MADS-box genes in rice, corn and wheat

Fig. 10 Co-linearity analysis of core MADS-box genes in tomato, potato and Etuberosum

References 40

[1]	Chen Y, Chu YF, Wang J, et al. Natural allelic variation in the CBF2 transcription factor is a pivotal factor controlling cold resistance in potato [J]. Plant Physiol, 2025, 199(2): kiaf428.
[2]	Bao XR, Zhu YK, Li GC, et al. Regulation of storage organ formation by long-distance tuberigen signals in potato [J]. Hortic Res, 2025, 12(4): uhae360.
[3]	Kondhare KR, Kumar A, Patil NS, et al. Development of aerial and belowground tubers in potato is governed by photoperiod and epigenetic mechanism [J]. Plant Physiol, 2021, 187(3): 1071-1086.
[4]	Dutta M, Mali S, Raturi V, et al. Transcriptional and post-transcriptional regulation of tuberization in potato (Solanum tuberosum L.) [J]. J Plant Growth Regul, 2024, 43(1): 11053.
[5]	Kondhare KR, Natarajan B, Banerjee AK. Molecular signals that govern tuber development in potato [J]. Int J Dev Biol, 2020, 64(1/2/3): 133-140.
[6]	Riechmann JL, Meyerowitz EM. MADS domain proteins in plant development [J]. Biol Chem, 1997, 378(10): 1079-1101.
[7]	Zhang ZH, Zou WH, Lin PX, et al. Evolution and function of MADS-box transcription factors in plants [J]. Int J Mol Sci, 2024, 25(24): 13278.
[8]	Hoffmann T, Shi XL, Hsu CY, et al. The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis [J]. BMC Plant Biol, 2022, 22: 18.
[9]	Zhang XN, Wang QJ, Yang SZ, et al. Identification and characterization of the MADS-box genes and their contribution to flower organ in carnation (Dianthus caryophyllus L.) [J]. Genes, 2018, 9(4): 193.
[10]	Liu RJ, Zhao D, Li PB, et al. Natural variation in OsMADS1 transcript splicing affects rice grain thickness and quality by influencing monosaccharide loading to the endosperm [J]. Plant Commun, 2025, 6(1): 101178.
[11]	Yang XL, Wu F, Lin XL, et al. Live and let die - the bsister MADS-box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa) [J]. PLoS One, 2012, 7(12): e51435.
[12]	Li CX, Lin HQ, Chen A, et al. WheatVRN1, FUL2 and FUL3 play critical and redundant roles in spikelet development and spike determinacy [J]. Development, 2019, 146(14): dev175398.
[13]	Su YL, Liu JX, Liang WQ, et al. Wheat AGAMOUS LIKE 6 transcription factors function in stamen development by regulating the expression of TaAPETALA3 [J]. Development, 2019: dev.177527.
[14]	Wu JR, Lawit SJ, Weers B, et al. Overexpression of zmm28 increases maize grain yield in the field [J]. Proc Natl Acad Sci U S A, 2019, 116(47): 23850-23858.
[15]	Kang SG, Hannapel DJ. A novel MADS-box gene of potato (Solanum tuberosum L.) expressed during the early stages of tuberization [J]. Plant Mol Biol, 1996, 31(2): 379-386.
[16]	Kang SC, Kang H. Characterization of potato vegetative MADS-Box gene, POTM1-1, in response to hormone applications [J]. J Plant Biol, 2002, 45(4): 196-200.
[17]	Carmona MJ, Ortega N, Garcia-Maroto F. Isolation and molecular characterization of a new vegetative MADS-box gene from Solanum tuberosum L [J]. Planta, 1998, 207(2): 181-188.
[18]	García-Maroto F, Ortega N, Lozano R, et al. Characterization of the potato MADS-box gene STMADS16 and expression analysis in tobacco transgenic plants [J]. Plant Mol Biol, 2000, 42(3): 499-513.
[19]	Wang YX, Ji XZ, Zhuang ZL, et al. Identification and bioinformatics analysis of MADS-box family genes containing K-box domain in maize [J]. Not Bot Horti Agrobo, 2023, 51(4): 13253.
[20]	Bharath SR, Mohan Raju B. Effect of varied levels of gibberellin, anti-gibberellin and cytokinin on growth and tuberization in potato [J]. Madras Agric J, 2024, 111: 35-44.
[21]	柳俊, 谢从华. 马铃薯块茎发育机理及其基因表达 [J]. 植物学通报, 2001, 18(5): 531-539.
	Liu J, Xie CH. The mechanism of potato (Solanum tuberosum L.) tuber development and related gene expression [J]. Chin Bull Bot, 2001, 18(5): 531-539.
[22]	Chen PL, Yang RX, Bartels D, et al. Roles of abscisic acid and gibberellins in stem/root tuber development [J]. Int J Mol Sci, 2022, 23(9): 4955.
[23]	Xu X, van Lammeren AAM, Vermeer E, et al. The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro 1 [J]. Plant Physiol, 1998, 117(2): 575-584.
[24]	Menzel CM. Tuberization in potato at high temperatures: responses to gibberellin and growth inhibitors [J]. Ann Bot, 1980, 46(3): 259-265.
[25]	Machida-Hirano R. Diversity of potato genetic resources [J]. Breed Sci, 2015, 65(1): 26-40.
[26]	Gao HH, Wang ZM, Li SL, et al. Genome-wide survey of potato MADS-box genes reveals that StMADS1 and StMADS13 are putative downstream targets of tuberigen StSP6A [J]. BMC Genom, 2018, 19: 726.
[27]	Tang dié, Jia YX, Zhang JZ, et al. Genome evolution and diversity of wild and cultivated potatoes [J]. Nature, 2022, 606(7914): 535-541.
[28]	van Lieshout N, van der Burgt A, de Vries ME, et al. Solyntus, the new highly contiguous reference genome for potato (Solanum tuberosum) [J]. G3, 2020, 10(10): 3489-3495.
[29]	Tang HB, Krishnakumar V, Zeng XF, et al. JCVI: a versatile toolkit for comparative genomics analysis [J]. iMeta, 2024, 3(4): e211.
[30]	刘计涛, 王梦诗, 索海翠, 等. 马铃薯GA2ox家族基因响应赤霉素(GA)和低温胁迫表达分析 [J]. 江苏农业学报, 2023, 39(5): 1110-1119.
	Liu JT, Wang MS, Suo HC, et al. Expression analysis of GA2ox family genes in response to gibberellin (GA) and cold stress in potato [J]. Jiangsu J Agric Sci, 2023, 39(5): 1110-1119.
[31]	尉瑞敏, 常燕楠, 庞鹏湘, 等. 马铃薯StZnT11的电子克隆、表达及生物信息学分析 [J]. 生物工程学报, 2020, 36(2): 362-371.
	Yu RM, Chang YN, Pang PX, et al. In silico cloning, expression and bioinformatics analysis of StZnT11 in Solanum tuberosum [J]. Chin J Biotechnol, 2020, 36(2): 362-371.
[32]	Zhong SF, Tian YF, Guan J, et al. Expression and function analyses of the MIKC^C-type MADS-box genes in Akebia trifoliata (Lardizabalaceae) flower development [J]. Acta Physiol Plant, 2024, 46(5): 52.
[33]	Ma ZM, Hu LJ, Jiang WZ. Understanding AP2/ERF transcription factor responses and tolerance to various abiotic stresses in plants: a comprehensive review [J]. Int J Mol Sci, 2024, 25(2): 893.
[34]	Huo SJ, Li YF, Li RP, et al. Genome-wide analysis of the MADS-box gene family in Rhododendron hainanense Merr. and expression analysis under heat and waterlogging stresses [J]. Ind Crops Prod, 2021, 172: 114007.
[35]	Arora R, Agarwal P, Ray S, et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress [J]. BMC Genom, 2007, 8: 242.
[36]	Ren LL, Sun HW, Dai SY, et al. Identification and characterization of MIKC^c-type MADS-box genes in the flower organs of Adonis amurensis [J]. Int J Mol Sci, 2021, 22(17): 9362.
[37]	Kang SG, Hannapel DJ, Suh SG. Potato MADS-box gene POTM1-1 transcripts are temporally and spatially distributed in floral organs and vegetative meristems [J]. Mol Cells, 2003, 15(1): 48-54.
[38]	Kaufmann K, Melzer R, Theißen G. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants [J]. Gene, 2005, 347(2): 183-198.
[39]	Fernandez JA, Habben JE, Schussler JR, et al. zmm28 transgenic maize increases both N uptake- and N utilization-efficiencies [J]. Commun Biol, 2022, 5: 555.
[40]	Lee S, Woo YM, Ryu SI, et al. Further characterization of a rice AGL12 group MADS-box gene, OsMADS26 [J]. Plant Physiol, 2008, 147(1): 156-168.