Genomic diversity, population structure, and genome-wide association reveal genetic differentiation and trait improvements in mango

Xiaowei Ma , Hongxia Wu , Bin Liu , Songbiao Wang , Yuehua Zhang , Muqing Su , Bin Zheng , Hongbing Pan , Bang Du , Jun Wang , Ping He , Qianfu Chen , Hong An , Wentian Xu , Xiang Luo

Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) : 153

PDF (1614KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) :153 DOI: 10.1093/hr/uhae153
Article
research-article
Genomic diversity, population structure, and genome-wide association reveal genetic differentiation and trait improvements in mango
Author information +
History +
PDF (1614KB)

Abstract

Mango ( Mangifera indica L.) has been widely cultivated as a culturally and economically significant fruit tree for roughly 4000 years. Despite its rich history, little is known about the crop’s domestication, genomic variation, and the genetic loci underlying agronomic traits. This study employs the whole-genome re-sequencing of 224 mango accessions sourced from 22 countries, with an average sequencing depth of 16.37 ×, to explore their genomic variation and diversity. Through phylogenomic analysis, M. himalis J.Y. Liang, a species grown in China, was reclassified into the cultivated mango group known as M. indica. Moreover, our investigation of mango population structure and differentiation revealed that Chinese accessions could be divided into two distinct gene pools, indicating the presence of independent genetic diversity ecotypes. By coupling genome-wide association studies with analyses of genotype variation patterns and expression patterns, we identified several candidate loci and dominant genotypes associated with mango flowering capability, fruit weight, and volatile compound production. In conclusion, our study offers valuable insights into the genetic differentiation of mango populations, paving the way for future agronomic improvements through genomic-assisted breeding.

Cite this article

Download citation ▾
Xiaowei Ma, Hongxia Wu, Bin Liu, Songbiao Wang, Yuehua Zhang, Muqing Su, Bin Zheng, Hongbing Pan, Bang Du, Jun Wang, Ping He, Qianfu Chen, Hong An, Wentian Xu, Xiang Luo. Genomic diversity, population structure, and genome-wide association reveal genetic differentiation and trait improvements in mango. Horticulture Research, 2024, 11 (7) : 153 DOI:10.1093/hr/uhae153

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was financially supported by the Natural Science Foundation of Guangdong Province (2021A1515010966), Hainan Provincial Natural Science Foundation of China (322CXTD524), Hainan Province Key Research and Development Plan (ZDYF2022XDNY255), National Natural Science Foundation of China (32360727), Guangdong Province Seed Industry Revitalization Project (2022-NPY-00-030), and China Agriculture Research System of MOF and MARA (CARS-31).

Author contributions

X.M. and X.L. performed the data analysis, prepared the figures, and drafted the manuscript. H.W., W. X., and S. W. provided support for data analysis. H.A, B.L., Y. Z., and B.Z. provide help for verification of the manuscript. M. S., P.H., and J.W. were in charge of field management and collected the samples. B.D., H. P., and Q. C. collected the phenotype data.

Data availability

The re-sequencing data of 224 accessions have been uploaded to the National Genomics Data Center (NGDC) with the BioProject accession PRJCA025449.

Conflict of interest statement:

The authors declare no conflict of interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Mukherjee SK. Origin of mango ( Mangifera indica ). Econ Bot. 1971; 8 :260-4

[2]

Wang P, Luo Y, Huang J. et al. The genome evolution and domestication of tropical fruit mango. Genome Biol. 2020; 21 :60

[3]

Eiadthong W, Yonemori K, Sugiura S. et al. Analysis of phylogenetic relationships in Mangifera by restriction site analysis of an amplified region of cpDNA. Sci Hortic. 1999; 80 :145-55

[4]

Warschefsky EJ, Von Wettberg EJB. Population genomic analysis of mango ( Mangifera indica ) suggests a complex history of domestication. New Phytol. 2019; 222 :2023-37

[5]

Olano CT, Schenell RJ, Quintanilla WE. et al. Pedigree analysis of Florida mango cultivars. Proc Fla State Hort Soc. 2005; 118 :192-7

[6]

Pandit SS, Chidley HG, Kulkarni RS. et al. Cultivar relationships in mango based on fruit volatile profiles. Food Chem. 2009; 114 :363-72

[7]

Shi S, Ma X, Xu W. et al. Evaluation of 28 mango genotypes for physicochemical characters, antioxidant capacity, and mineral content. J Appl Bot Food Qual. 2015; 88 :264-73

[8]

Dillon NL, Bally ISE, Wright CL. et al. Genetic diversity of the Australian national mango gene bank. Sci Hortic. 2013; 150 :213-26

[9]

Dag A, Gazit S, Eisenstein D. et al. Effect of the male parent on pericarp and seed weights in several Floridian mango cultivars. Sci Hortic. 1999; 82 :325-9

[10]

Lavi U, Tomer E, Gazit S. et al. Components of the genetic variance and genetic correlations between traits in mango. Sci Hortic. 1998; 75 :11-25

[11]

Tasi CC, Chen YH, Chen CH. et al. Cultivar identification and genetic relationship of mango ( Mangifera indica ) in Taiwan using 37 SSR markers. Sci Hortic. 2013; 164 :196-201

[12]

Adato A, Sharon D, Lavi U. et al. Application of DNA fingerprints for identification and genetic analyses of mango ( Mangifera indica ) genotypes. J Amer Soc Hort Sci. 1995; 120 :259-64

[13]

Khalil K, Fang JG, Tomer E. et al. Cultivar identification and genetic map of mango ( Mangifera indica ). Euphytica. 2001; 122 :129-36

[14]

He XH, Guo YZ, Li YR. et al. Assessment of the genetic relationship and diversity of mango and its relatives by cplSSR marker. Agric Sci in China. 2007; 6 :137-42

[15]

Xiang L, Zhou HJ, Cao D. et al. Domestication and selection footprints in Persian walnuts ( Juglans regia ). PLoS Genet. 2022; 18 :e1010513

[16]

Li Y, Cao K, Zhu GR. et al. Genomic analyses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history. Genome Biol. 2019; 20 :36

[17]

Wu J, Wang YT, Xu JB. et al. Diversification and independent domestication of Asian and European pears. Genome Biol. 2018; 19 :77

[18]

Wu GA, Terol J, Ibanez V. et al. Genomics of the origin and evolution of citrus. Nature. 2018; 554 :311-6

[19]

Li W, Zhu XG, Zhang QJ. et al. SMAT sequencing generates the chromosome-scale reference genome of tropical fruit mango, Mangifera indica. BioRxiv. 2020; 2 :960880. Preprint: not peer reviewed.

[20]

Bally ISE, Bombarely A, Chambers AH. et al. The ‘Tommy Atkins’ mango genome reveals candidate genes for fruit quality. BMC Plant Biol. 2021; 21 :108

[21]

Ma XW, Luo X, Wei YZ. et al. Chromosome-scale genome and comparative transcriptomic analysis reveal transcriptional regulators of β -carotene biosynthesis in mango. Front Plant Sci. 2021; 12 :749108

[22]

Eckert AJ, Wegrzyn JL, Cumbie WP. et al. Association genetics of the loblolly pine ( Pinus taeda, Pinaceae) metabolome. New Phytol. 2012; 193 :890-902

[23]

Parchman TL, Gompert Z, Mudge J. et al. Genome-wide association genetics of an adaptive trait in lodgepole pine. Mol Ecol. 2012; 21 :2991-3005

[24]

Olson MS, Levsen N, Soolanayakanahally RY. et al. The adaptive potential of Populus balsamifera L. to phenology requirements in a warmer global climate. Mol Ecol. 2013; 22 :1214-30

[25]

Cingolani P, Platts A, Wang L. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms. SnpEff Fly. 2012; 6 :80-92

[26]

Yuan GZ, Wu Z, Liu XY. et al. Characterization and functional analysis of LoUDT1, a bHLH transcription factor related to anther development in the lily oriental hybrid Siberia ( Lilium spp.). Plant Physiol Bioch. 2021; 166 :1087-95

[27]

Ye LX, Wu YM, Zhang JX. et al. A bZIP transcription factor (CiFD) regulates drought- and low-temperature-induced flowering by alternative splicing in citrus. J Integr Plant Biol. 2022; 3 :674-91

[28]

Liang JH, Wu Z, Xu TF. et al. Overexpression of HANABA TARANU in cultivated strawberry delays flowering and leads to defective flower and fruit development. Plant Sci. 2022; 321 :111307

[29]

Du SS, Li L, Li L. et al. Photoexcited cryptochrome2 interacts directly with TOE1 and TOE2 in flowering regulation. Plant Physiol. 2020; 184 :487-505

[30]

Kosentka PZ, Overholt A, Maradiaga R. et al. EPFL signals in the boundary region of the SAM restrict its size and promote leaf initiation. Plant Physiol. 2019; 179 :265-79

[31]

Bessho-Uehara K, Wang DR, Furuta T. et al. Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. Proc Natl Acad Sci USA. 2016; 113 :8969-74

[32]

Szécsi J, Joly C, Bordji K. et al. BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J. 2006; 25 :3912-20

[33]

Li X, Xu YY, Shen SL. et al. Transcription factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit. J Exp Bot. 2017; 68 :4929-38

[34]

Luo C, Shu B, Yao QS. et al. Construction of high-density genetic map based on large-scale marker development in mango using specific-locus amplified fragment sequencing. Front Plant Sci. 2016; 7 :1310

[35]

Zhan RL, Wang SB, Wu HX. et al. Cultivation and Pest Management of Mango. Beijing: Agricultural Press of China; 2023:

[36]

Dai FW, Zhou XK, Luo GQ. et al. Genomic resequencing unravels the genetic basis of domestication, expansion, and trait improvement in Morus Atropurpurea. Adv Sci. 2023; 10 :2370161

[37]

Cao K, Li Y, Deng CH. et al. Comparative population genomics identified genomic regions and candidate genes associated with fruit domestication traits in peach. Plant Biotechnol J. 2019; 17 :1954-70

[38]

Cao K, Wang B, Fang WC. et al. Combined nature and human selections reshaped peach fruit metabolome. Genome Biol. 2022; 23 :146

[39]

Chunwongse C, Phumichai C, Tongyoo P. et al. Development of di-nucleotide microsatellite markers and construction of genetic linkage mapping mango ( Mangifera indica L.). Songkalankarin J Sci Technol. 2015; 37 :119-27

[40]

Chunwongse C, Phumichai C, Barbarasert C. et al. Molecular mapping of mango cultivars ‘alphonso’ and ‘palmer’. Acta Hortic. 2000; 509 :193-206

[41]

Fang JG, Liu DJ, Ma ZQ.Constructing mango ( Mangifer indica L.) genetic map using markers for double heterozygous loci. Mol Plant Breed. 2003; 1 :313-9

[42]

Kashkush K, Fang J, Eli T. et al. Cultivar identification and genetic map of mango ( Mangifera indica ). Euphytia. 2001; 122 :129-36

[43]

Wang MY, Gao M, Zhao YX. et al. LcERF19, an AP2/ERF transcription factor from Litsea cubeba, positively regulates geranial and neral biosynthesis. Hortic Res. 2022; 9 :uhab093

[44]

Li S, Wang H, Li F. et al. The maize transcription factor EREB58 mediates the jasmonate-induced production of sesquiterpene volatiles. Plant J. 2015; 84 :296-308

[45]

Duan N, Bai Y, Sun H. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun. 2017; 8 :249

[46]

Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980; 8 :4321-6

[47]

Patel RK, Jain M. NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One. 2012; 7 :e30619

[48]

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25 :1754-60

[49]

DePristo MA, Banks E, Poplin R. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011; 43 :491-8

[50]

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009; 19 :1655-64

[51]

Kamvar ZN, Tabima JF, Grunwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014; 2 :e281

[52]

Danecek P, Auton A, Abecasis G. et al. The variant call format and VCF tools. Bioinformatics. 2011; 27 :2156-8

[53]

Zhang C, Dong SS, Xu JY. et al. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019; 35 :1786-8

[54]

Ma XW, Su MQ, Wu HX. et al. Analysis of the volatile profile of core Chinese mango germplasm by headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry. Molecules. 2018; 23 :1480

[55]

Lippert C, Listgarten J, Liu Y. et al. FaST linear mixed models for genome-wide association studies. Nat Methods. 2011; 8 :833-5

[56]

Liu X, Huang M, Fan B. et al. Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. 2016; 12 :e1005767

[57]

Bolger A, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30 :2114-20

[58]

Kim D, Pertea G, Trapnell C. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14 :R36-13

[59]

Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12 :323

PDF (1614KB)

90

Accesses

0

Citation

Detail

Sections
Recommended

/