Jackfruit genome and population genomics provide insights into fruit evolution and domestication history in China

Abstract

As the largest known tree-borne fruit in the world, jackfruit (Artocarpus heterophyllus) is an important cultivated crop in tropical regions of South and Southeast Asia. The species has been cultivated in China for more than 1000 years, but the history of its introduction to the country remains unclear. We assembled a high-quality chromosome-level genome of jackfruit into 985.63 Mb with scaffold N50 of 32.81 Mb. We analyzed whole-genome resequencing data of 295 landraces to investigate the domestication history in China and agronomic trait evolution of jackfruit. Population structure analysis revealed that jackfruits of China could be traced back to originate from Southeast Asia and South Asia independently. Selection signals between jackfruit and its edible congener, cempedak (Artocarpus integer), revealed several important candidate genes associated with fruit development and ripening. Moreover, analyses of selective sweeps and gene expression revealed that the AhePG1 gene may be the major factor in determining fruit texture. This study not only resolves the origins of jackfruit of China, but also provides valuable genomic resources for jackfruit breeding improvement and offers insights into fruit size evolution and fruit texture changes.

References

[1] Zerega NJC, Supardi MNN, Motley TJ . Phylogeny and recircumscription of Artocarpeae (Moraceae) with a focus on Artocarpus . Syst Bot. 2010; 35: 766-82.

[2] Ranasinghe RASN, Maduwanthi SDT, Marapana RAUJ . Nutritional and health benefits of jackfruit (Artocarpus heterophyllus Lam.): a review . Int J Food Sci. 2019; 2019: 4327183.

[3] Tiwari AK, Vidyarthi AS . Nutritional evaluation of various edible fruit parts of jackfruit (Artocarpus heterophyllus) at different maturity stages . Int J Chem Pharm Rev Res. 2015; 1: 21-6.

[4] Bangladesh Bureau of Statistics . Statistical Yearbook of Bangladesh 2017, 37th edn. Dhaka: Statistics and Information Division, Ministry of Planning Government of the People’s Republic of Bangladesh, 2018.

[5] Altendorf S . Minor tropical fruits. Food Outlook. 2018; July: 67-74.

[6] Ajayi IA . Use of jackfruit (Artocarpus heterophyllus) seeds in health . In: Preedy VR, Watson RR, Patel VB, eds. Nuts and Seeds in Health and Disease Prevention.Oxford: Elsevier, 2011, 677-83.

[7] Khan R, Zerega N, Hossain S et al. Jackfruit (Artocarpus heterophyllus Lam.) diversity in Bangladesh: land use and artificial selection . Econ Bot. 2010; 64: 124-36.

[8] Jarrett FM . Studies in Artocarpus and allied genera, III. A revision of Artocarpus subgenus Artocarpus . J Arnold Arbor. 1959; 40: 327-68.

[9] Jagadeesh SL, Reddy BS, Swamy GSK et al. Chemical composition of jackfruit (Artocarpus heterophyllus Lam.) selections of Western Ghats of India . Food Chem. 2007; 102: 361-5.

[10] Barrau J . Breadfruit and relatives. In: Simmonds NW, ed. Evolution of Crop Plants.London: Longmans, 1976, 201-2.

[11] Williams EW, Gardner EM, Harris R III et al. Out of Borneo: biogeography, phylogeny and divergence date estimates of Artocarpus (Moraceae). Ann Bot. 2017;119:611-27.

[12] Hu WL, Wang SM . On jackfruits’ introduction, dispersal and reasons for planting in China. Agricultural History of China 2016; 5: 30-9. [In Chinese.]

[13] Haq N. Jackfruit: Artocarpus heterophyllus (Fruits for the Future) . Southampton: University of Southampton, International Centre for Underutilised Crops; 2006.

[14] Wu G, Chen HP, Sang LW et al. Status of jackfruit industry in China and development countermeasures. Chinese J Trop Agric 2013; 33: 91-7. [In Chinese.]

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

[16] Feng C, Feng C, Lin XG et al. A chromosome-level genome assembly provides insights into ascorbic acid accumulation and fruit softening in guava (Psidium guajava) . Plant Biotechnol J. 2021; 19: 717-30.

[17] Liao L, Zhang WH, Zhang B et al. Unraveling a genetic roadmap for improved taste in the domesticated apple. Mol Plant. 2021; 14: 1454-71.

[18] Yu Y, Guan JT, Xu YG et al. Population-scale peach genome analyses unravel selection patterns and biochemical basis underlying fruit flavor. Nat Commun. 2021; 12: 3604.

[19] Zhang Q, Onstein RE, Little SA et al. Estimating divergence times and ancestral breeding systems in Ficus and Moraceae. Ann Bot. 2019; 123: 191-204.

[20] Soltis PS, Soltis DE . Ancient WGD events as drivers of key innovations in angiosperms. Curr Opin Plant Biol. 2016; 30: 159-65.

[21] de Almeida Lopes MM, de Souza KO, de Oliveira Silva E . Cempedak- Artocarpus champeden . In: S. Rodrigues, E. de Oliveira Silva, E. Sousa de Brito, eds. Exotic Fruits Reference Guide.Oxford: Elsevier, 2018; 121-7.

[22] Wang MMH, Gardner EM, Chung RCK et al. Origin and diversity of an underutilized fruit tree crop, cempedak (Artocarpus integer, Moraceae) . Am J Bot. 2018; 105: 898-914.

[23] Chen XY, Kim JY . Callose synthesis in higher plants. Plant Signal Behav. 2009; 4: 489-92.

[24] Cui W, Lee JY . Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress . Nat Plants. 2016; 2: 16034.

[25] Gil P, Dewey E, Friml J et al. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis . Genes Dev. 2001; 15: 1985-97.

[26] Chen LQ, Qu XQ, Hou BH et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012; 335: 207-11.

[27] Xu FQ, Xue HW . The ubiquitin-proteasome system in plant responses to environments. Plant Cell Environ. 2019; 42: 2931-44.

[28] Rahman AKMM, Huq E, Mian AJ et al. Microscopic and chemical changes occurring during the ripening of two forms of jackfruit (Artocarpus heterophyllus L.) . Food Chem. 1995; 52: 405-10.

[29] Ferrer-Admetlla A, Liang M, Korneliussen T et al. On detecting incomplete soft or hard selective sweeps using haplotype structure. Mol Biol Evol. 2014; 31: 1275-91.

[30] Turner-Hissong SD, Mabry ME, Beissinger TM et al. Evolutionary insights into plant breeding. Curr Opin Plant Biol. 2020; 54: 93-100.

[31] Wang DD, Yeats TH, Uluisik S et al. Fruit softening: revisiting the role of pectin. Trends Plant Sci. 2018; 23: 302-10.

[32] Fu MZ . Revisiting ancient silk roads: origin and evolution. Pacific J. 2017; 25: 59-74. [In Chinese.]

[33] Robert NS III . Fruit from the Sands: The Silk Road Origins of the Foods we Eat . Oakland: University of California Press; 2019.

[34] Frankopan P . The Silk Roads: A New History of the World . London: Bloomsbury Publishing; 2015.

[35] Sun H, Min R, Wang YC . The east route of the silk road in South Asia: the heritage range, development process, important roads and their significance. Archaeological Research of the Silk Road. 2020; 11: 338-78. [In Chinese.]

[36] Mukherjee SK . The mango and its wild relatives. Sci Cult. 1949; 26: 5-9.

[37] Li SL . A study on the geographical distribution of ancient jackfruit. Agric Archaeol 2012; 3: 191- 3. [In Chinese.]

[38] Verma DPS, Hong ZL . Plant callose synthase complexes. Plant Mol Biol. 2001; 47: 693-701.

[39] Dong XY, Hong ZL, Sivaramakrishnan M et al. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis . Plant J. 2005; 42: 315-28.

[40] Mijin S, Ding P . Growth development and structural changes of Malaysian jackfruit cv. Tekam yellow syncarp. Sci Hortic. 2020; 272: 109594.

[41] Mijin S, Ding P, Saari N et al. Effects of pollination techniques and harvesting stage on the physico-chemical characteristics of jackfruit. Sci Hortic. 2021; 285: 110199.

[42] Li YZ, Mao Q, Feng F et al. Genetic diversity within a jackfruit (Artocarpus heterophyllus Lam.) germplasm collection in China using AFLP markers . Agric Sci China. 2010; 9: 1263-70.

[43] Quesada MA, Blanco-Portales R, Pose S et al. Antisense downregulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol. 2009; 150: 1022-32.

[44] Atkinson RG, Sutherland PW, Johnston SL et al. Down-regulation of POLYGALACTURONASE1 alters firmness, tensile strength and water loss in apple (Malus x domestica) fruit . BMC Plant Biol. 2012; 12: 129.

[45] Morgutti S, Negrini N, Nocito FF et al. Changes in enclopolygalacturonase levels and characterization of a putative endo-PG gene during fruit softening in peach genotypes with nonmelting and melting flesh fruit phenotypes. New Phytol. 2006; 171: 315-28.

[46] Ghiani A, Onelli E, Aina R et al. A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endo-polygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. J Exp Bot. 2011; 62: 4043-54.

[47] Gu C, Wang L, Wang W et al. Copy number variation of a gene cluster encoding endopolygalacturonase mediates flesh texture and stone adhesion in peach. J Exp Bot. 2016; 67: 1993-2005.

[48] Dong LL, Wang YB, Li YZ et al. Activity of glycosidase and polygalacturonase in jackfruit fruit. J Southern Agric 2013; 44: 924-9. [In Chinese.]

[49] Chin CS, Peluso P, Sedlazeck FJ et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 2016; 13: 1050-4.

[50] Chin CS, Alexander DH, Marks P et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods. 2013; 10: 563-9.

[51] Walker BJ, Abeel T, Shea T et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014; 9: e112963.

[52] Adey A, Kitzman JO, Burton JN et al. In vitro, long-range sequence information for de novo genome assembly via transposase contiguity. Genome Res. 2014; 24: 2041-9.

[53] Langmead B, Salzberg SL . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9: 357-9.

[54] Liu B, Shi Y, Yuan J et al. Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects . Preprint at https://doi.org/10.48550/arXiv.1308.2012.

[55] Parra G, Bradnam K, Korf I . CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics. 2007; 23: 1061-7.

[56] Simao FA, Waterhouse RM, Ioannidis P et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31: 3210-2.

[57] Emms DM, Kelly S . OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015; 16: 157.

[58] Edgar RC . MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7.

[59] Nguyen LT, Schmidt HA, von Haeseler A et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32: 268-74.

[60] Mirarab S, Warnow T . ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics. 2015; 31: i44-52.

[61] Drummond AJ, Suchard MA, Xie D et al. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012; 29: 1969-73.

[62] De Bie T, Cristianini N, Demuth JP et al. CAFE: a computational tool for the study of gene family evolution. Bioinformatics. 2006; 22: 1269-71.

[63] Yu G, Wang LG, Han Y et al. Cluster profiler: an R package for comparing biological themes among gene clusters. OMICS. 2012; 16: 284-7.

[64] Tang H, Bowers JE, Wang X et al. Synteny and collinearity in plant genomes. Science. 2008; 320: 486-8.

[65] Darzentas N. Circoletto: visualizing sequence similarity with Circos. Bioinformatics. 2010; 26: 2620-1.

[66] Zwaenepoel A, Van de Peer Y . Wgd-simple command line tools for the analysis of ancient whole-genome duplications. Bioinformatics. 2019; 35: 2153-5.

[67] Feng C, Xu M, Feng C et al. The complete chloroplast genome of Primulina and two novel strategies for development of high polymorphic loci for population genetic and phylogenetic studies. BMC Evol Biol. 2017; 17: 224.

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

[69] Li H, Handsaker B, Wysoker A et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25: 2078-9.

[70] McKenna A, Hanna M, Banks E et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20: 1297-303.

[71] Danecek P, Auton A, Abecasis G et al. The variant call format and VCFtools. Bioinformatics. 2011; 27: 2156-8.

[72] Purcell S, Neale B, Todd-Brown K et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81: 559-75.

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

[74] 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.

[75] Pickrell JK, Pritchard JK . Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012; 8: e1002967.

[76] Malinsky M, Matschiner M, Svardal H . Dsuite-fast D-statistics and related admixture evidence from VCF files. Mol Ecol Resour. 2021; 21: 584-95.

[77] Browning BL, Browning SR . Improving the accuracy and efficiency of identity-by-descent detection in population data. Genetics. 2013; 194: 459-71.

[78] Han F, Lamichhaney S, Grant BR et al. Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin’s finches. Genome Res. 2017; 27: 1004-15.

[79] Sabeti PC, Varilly P, Fry B et al. Genome-wide detection and characterization of positive selection in human populations. Nature. 2007; 449: 913-8.

[80] Szpiech ZA, Novak TE, Bailey NP et al. Application of a novel haplotype-based scan for local adaptation to study high-altitude adaptation in rhesus macaques. Evol Lett. 2021; 5: 408-21.

[81] Voight BF, Kudaravalli S, Wen XQ et al. A map of recent positive selection in the human genome. PLoS Biol. 2006; 4: e72.

[82] Szpiech ZA, Hernandez RD . Selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol Biol Evol. 2014; 31: 2824-7.

[83] Pertea M, Kim D, Pertea GM et al. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; 11: 1650-67.