Abstract
It is an intriguing issue of evolutionary biology how genetic diversity and gene expression diversity shape the adaptive patterns. Comparative transcriptomic studies of wild populations in extreme environments provide critical insights into the relative contribution of genetic and expressive components. In this study, we analyzed the genetic diversity and gene expression diversity of 20 populations of the aquatic plant Batrachium bungei along elevations ranging from 2690 to 4896 m on the Qinghai–Tibet plateau (QTP). Based on single nucleotide polymorphisms (SNPs) and gene expression data from 100 individuals of B. bungei, we found that variation in genetic sequence was more sensitive to detect weak differentiation than gene expression. Using 292,613 high-quality SNPs, we documented a significant phylogeographical structure, a low within-population genetic diversity, and a high inter-population genetic differentiation in B. bungei populations. Analysis of relationship between geographic distance, genetic distance, and gene expression similarity showed that geographic isolation shaped gene flow patterns but not gene expression patterns. We observed a negative relationship between genetic diversity and gene expression diversity within and among B. bungei populations, and we demonstrated that as environmental conditions worsen with increasing altitude, genetic diversity played an increased role in maintaining the stability of populations, while the corresponding role of gene expression diversity decreased. These results suggested that genetic diversity and gene expression diversity might act as a complementary mechanism contributing to the long-term survival of B. bungei in extreme environments.
Key message
Genetic diversity and gene expression diversity might act as a complementary mechanism contributing to the long-term survival of B. bungei in extreme environments.
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Data availability
The RNA sequencing data generated in this work have been deposited to the NCBI’s Sequence Read Archive under accession number SRR18512371-SRR18512470 (BioProject PRJNA820952) (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA820952).
References
Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinform 12:246. https://doi.org/10.1186/1471-2105-12-246
Alvarez M, Schrey AW, Richards CL (2015) Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution? Mol Ecol 24(4):710–725. https://doi.org/10.1111/mec.13055
Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc Biol Sci 272(1566):877–886. https://doi.org/10.1098/rspb.2004.3045
Benavides R, Carvalho B, Matesanz S, Bastias CC, Cavers S, Escudero A et al (2021) Phenotypes of Pinus sylvestris are more coordinated under local harsher conditions across Europe. J Ecol 109(7):2580–2596. https://doi.org/10.1111/1365-2745.13668
Bornette G, Puijalon S (2011) Response of aquatic plants to abiotic factors: a review. Aquat Sci 73(1):1–14. https://doi.org/10.1007/s00027-010-0162-7
Brauer CJ, Unmack PJ, Beheregaray LB (2017) Comparative ecological transcriptomics and the contribution of gene expression to the evolutionary potential of a threatened fish. Mol Ecol 26(24):6841–6856. https://doi.org/10.1111/mec.14432
Brook B (2004) Population ecology: first principles. Austral Ecol 29:684–685. https://doi.org/10.1111/j.1442-9993.2004.01359.x
Caruana BM, Pembleton LW, Constable F, Rodoni B, Slater AT, Cogan NOI (2019) Validation of genotyping by sequencing using transcriptomics for diversity and application of genomic selection in tetraploid potato. Front Plant Sci 10:670. https://doi.org/10.3389/fpls.2019.00670
Chen JH, Du ZY, Yuan YH, Wang QF (2014) Phylogeography of an alpine aquatic herb Ranunculus bungei (Ranunculaceae) on the Qinghai–Tibet Plateau. J Syst Evol 52(3):313–325. https://doi.org/10.1111/jse.12093
Chen LY, Zhao SY, Wang QF, Moody ML (2015) Transcriptome sequencing of three Ranunculus species (Ranunculaceae) reveals candidate genes in adaptation from terrestrial to aquatic habitats. Sci Rep 5:10098. https://doi.org/10.1038/srep10098
Chien WM, Chang CT, Chiang YC, Hwang SY (2020) Ecological factors generally not altitude related played main roles in driving potential adaptive evolution at elevational range margin populations of Taiwan Incense Cedar (Calocedrus formosana). Front Genet 11:580630. https://doi.org/10.3389/fgene.2020.580630
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al (2011) The variant call format and VCF tools. Bioinformatics 27(15):2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Dayan DI, Crawford DL, Oleksiak MF (2015) Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus. Mol Ecol 24(13):3345–3359. https://doi.org/10.1111/mec.13188
De Kort H, Prunier JG, Ducatez S, Honnay O, Baguette M, Stevens VM et al (2021) Life history, climate and biogeography interactively affect worldwide genetic diversity of plant and animal populations. Nat Commun 12(1):516. https://doi.org/10.1038/s41467-021-20958-2
de Villemereuil P, Mouterde M, Gaggiotti OE, Till-Bottraud I (2018) Patterns of phenotypic plasticity and local adaptation in the wide elevation range of the alpine plant Arabis alpina. J Ecol 106(5):1952–1971. https://doi.org/10.1111/1365-2745.12955
DeBiasse MB, Kelly MW (2016) Plastic and evolved responses to global change: what can we learn from comparative transcriptomics? J Hered 107(1):71–81. https://doi.org/10.1093/jhered/esv073
Dennison W, Orth R, Moore K, Stevenson J, Carter V, Kollar S et al (1993) Assessing water quality with submersed aquatic vegetation. BioScience 43:86–94. https://doi.org/10.2307/1311969
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491–498. https://doi.org/10.1038/ng.806
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20
Flora of China (2021) http://www.iplant.cn/. accessed 20
Frei ER, Ghazoul J, Matter P, Heggli M, Pluess AR (2014) Plant population differentiation and climate change: responses of grassland species along an elevational gradient. Glob Change Biol 20(2):441–455. https://doi.org/10.1111/gcb.12403
Gibson G (2008) The environmental contribution to gene expression profiles. Nat Rev Genet 9(8):575–581. https://doi.org/10.1038/nrg2383
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883
Guggisberg A, Lai Z, Huang J, Rieseberg LH (2013) Transcriptome divergence between introduced and native populations of Canada thistle, Cirsium arvense. New Phytol 199(2):595–608. https://doi.org/10.1111/nph.12258
Hamann E, Pauli CS, Joly-Lopez Z, Groen SC, Rest JS, Kane NC et al (2021) Rapid evolutionary changes in gene expression in response to climate fluctuations. Mol Ecol 30(1):193–206. https://doi.org/10.1111/mec.15583
Hughes AR, Inouye BD, Johnson MT, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11(6):609–623. https://doi.org/10.1111/j.1461-0248.2008.01179.x
Jiang L, Zheng Z, Qi T, Kemper KE, Wray NR, Visscher PM et al (2019) A resource-efficient tool for mixed model association analysis of large-scale data. Nat Genet 51(12):1749–1755. https://doi.org/10.1038/s41588-019-0530-8
Kenkel CD, Matz MV (2016) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat Ecol Evol 1(1):14. https://doi.org/10.1038/s41559-016-0014
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36. https://doi.org/10.1186/gb-2013-14-4-r36
Körner C (2003) Alpine plant life. Springer, Berlin
Korner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22(11):569–574. https://doi.org/10.1016/j.tree.2007.09.006
Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R et al (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15(4):378–392. https://doi.org/10.1111/j.1461-0248.2012.01746.x
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Lasky JR, Des Marais DL, Lowry DB, Povolotskaya I, McKay JK, Richards JH et al (2014) Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana. Mol Biol Evol 31(9):2283–2296. https://doi.org/10.1093/molbev/msu170
Levin DA (2010) Environment-enhanced self-fertilization: implications for niche shifts in adjacent populations. J Ecol 98(6):1276–1283. https://doi.org/10.1111/j.1365-2745.2010.01715.x
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. https://doi.org/10.1186/1471-2105-12-323
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659. https://doi.org/10.1093/bioinformatics/btl158
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al (2009) The sequence alignment/Map format and SAM tools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu W, Kang L, Xu Q, Tao C, Yan J, Sang T (2019) Increased expression diversity buffers the loss of adaptive potential caused by reduction of genetic diversity in new unfavourable environments. Biol Lett 15(1):20180583. https://doi.org/10.1098/rsbl.2018.0583
Liu Q, Xie Y, Liu B, Huanhuan Z, Feng Z et al (2020) A transcriptomic variation map provides insights into the genetic basis of Pinus massoniana Lamb. Evolution and the association with oleoresin yield. BMC Plant Biol 20(1):375. https://doi.org/10.1186/s12870-020-02577-z
Liu L, Wang Z, Su Y, Wang T (2021) Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae). BMC Genomics 22(1):388. https://doi.org/10.1186/s12864-021-07682-3
Losos JB (2011) Convergence, adaptation, and constraint. Evolution 65(7):1827–1840. https://doi.org/10.1111/j.1558-5646.2011.01289.x
Lustenhouwer N, Williams JL, Levine JM (2019) Evolution during population spread affects plant performance in stressful environments. J Ecol 107(1):396–406. https://doi.org/10.1111/1365-2745.13045
Ma Y, Wang J, Hu Q, Li J, Sun Y, Zhang L et al (2019) Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex. Commun Biol 2:213. https://doi.org/10.1038/s42003-019-0445-z
Mao KS, Wang Y, Liu JQ (2021) Evolutionary origin of species diversity on the Qinghai–Tibet plateau. J Syst Evol 59(6):1142–1158. https://doi.org/10.1111/jse.12809
McGaughran A, Laver R, Fraser C (2021) Evolutionary responses to warming. Trends Ecol Evol 36(7):591–600. https://doi.org/10.1016/j.tree.2021.02.014
Nathan R (2006) Long-distance dispersal of plants. Science 313(5788):786–788. https://doi.org/10.1126/science.1124975
Ntuli NN, Nicastro KR, Zardi GI, Assis J, McQuaid CD, Teske PR (2020) Rejection of the genetic implications of the “Abundant centre Hypothesis” in marine mussels. Sci Rep 10(1):604. https://doi.org/10.1038/s41598-020-57474-0
Pavlova A, Beheregaray LB, Coleman R, Gilligan D, Harrisson KA, Ingram BA et al (2017) Severe consequences of habitat fragmentation on genetic diversity of an endangered australian freshwater fish: a call for assisted gene flow. Evol Appl 10(6):531–550. https://doi.org/10.1111/eva.12484
Qu Y, Chen C, Xiong Y, She H, Zhang YE, Cheng Y et al (2020) Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in eurasian tree sparrows. Natl Sci Rev 7(1):113–127. https://doi.org/10.1093/nsr/nwz138
Richards CL, Hanzawa Y, Katari MS, Ehrenreich IM, Engelmann KE, Purugganan MD (2009) Perspective on ecological and evolutionary systems biology. Annu Rev Plant Biol 35:331–351
Rivera HE, Aichelman HE, Fifer JE, Kriefall NG, Wuitchik DM, Wuitchik SJS et al (2021) A framework for understanding gene expression plasticity and its influence on stress tolerance. Mol Ecol 30(6):1381–1397. https://doi.org/10.1111/mec.15820
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22(9):454–464. https://doi.org/10.1016/j.tree.2007.07.002
Romero IG, Ruvinsky I, Gilad Y (2012) Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet 13(7):505–516. https://doi.org/10.1038/nrg3229
Santamaría L (2002) Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecol 23(3):137–154. https://doi.org/10.1016/s1146-609x(02)01146-3
Shen Y, Xia H, Tu Z, Zong Y, Yang L, Li H (2022) Genetic divergence and local adaptation of Liriodendron driven by heterogeneous environments. Mol Ecol 31(3):916–933. https://doi.org/10.1111/mec.16271
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31(19):3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S (2016) TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res 26(8):1134–1144. https://doi.org/10.1101/gr.196469.115
Sovic M, Fries A, Martin SA, Lisle Gibbs H (2019) Genetic signatures of small effective population sizes and demographic declines in an endangered rattlesnake, Sistrurus catenatus. Evol Appl 12(4):664–678. https://doi.org/10.1111/eva.12731
VanWallendael A, Soltani A, Emery NC, Peixoto MM, Olsen J, Lowry DB (2019) A molecular view of plant local adaptation: incorporating stress-response networks. Annu Rev Plant Biol 70(29):559–583. https://doi.org/10.1146/annurev-arplant-050718-100114
Vences M, Hauswaldt JS, Steinfartz S, Rupp O, Goesmann A, Kunzel S et al (2013) Radically different phylogeographies and patterns of genetic variation in two European brown frogs, genus Rana. Mol Phylogenet Evol 68(3):657–670. https://doi.org/10.1016/j.ympev.2013.04.014
Wang YH, Chen JM, Xu C, Liu X, Wang QF, Motley TJ (2010) Population genetic structure of an aquatic herb Batrachium bungei (Ranuculaceae) in the Hengduan Mountains of China. Aquat Bot 92(3):221–225. https://doi.org/10.1016/j.aquabot.2009.12.004
Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV et al (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20(9):1377–1419. https://doi.org/10.1093/molbev/msg140
Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31:39–59
Wu Z, Xu X, Zhang J, Wiegleb G, Hou H (2019) Influence of environmental factors on the genetic variation of the aquatic macrophyte Ranunculus subrigidus on the Qinghai–Tibetan Plateau. BMC Evol Biol 19(1):228. https://doi.org/10.1186/s12862-019-1559-0
Xu Q, Xing S, Zhu C, Liu W, Fan Y, Wang Q et al (2015) Population transcriptomics reveals a potentially positive role of expression diversity in adaptation. J Integr Plant Biol 57(3):284–299. https://doi.org/10.1111/jipb.12287
Yan J, Zhu MD, Liu W, Xu Q, Zhu CY, Li JQ et al (2016) Genetic variation and bidirectional gene flow in the riparian plant Miscanthus lutarioriparius, across its endemic range: implications for adaptive potential. Glob Change Biol Bioenergy 8(4):764–776. https://doi.org/10.1111/gcbb.12278
Yan J, Song Z, Xu Q, Kang L, Zhu C, Xing S et al (2017) Population transcriptomic characterization of the genetic and expression variation of a candidate progenitor of Miscanthus energy crops. Mol Ecol 26(21):5911–5922. https://doi.org/10.1111/mec.14338
Yang MX, Wang XJ, Pang GJ, Wang GN, Liu ZC (2019) The Tibetan Plateau cryosphere: observations and model simulations for current status and recent changes. Earth Sci Rev 190:353–369. https://doi.org/10.1016/j.earscirev.2018.12.018
Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y et al (2011) High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc 2011(8):940–949. https://doi.org/10.1101/pdb.prot5652
Acknowledgements
This work was supported in part by the National Natural Science Foundation of China (31860046), and Plateau Ecology Youth Innovative Fund of Wuhan University (413100105). We sincerely thank Wenkai Li from China University of Geoscience for his critical help on data visualization. Additionally, we also thank Liya Ji, Guoqi Xu, Xuanfeng Wu, Xinzhong Li and Pincuo Zhaxi from Tibet University for their critical assistance on sample collection.
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Funding was provided by National Natural Science Foundation of China (Grant No. 31860046).
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XL and XL conceived the study. XY completed the data analysis with the help of FC, ZC, PW, CL and XS helped with the data visualization. TL and FC collected the samples, and XY wrote the manuscript with the help of XL.
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Yu, X., Chen, F., Chen, Z. et al. Genetic diversity and gene expression diversity shape the adaptive pattern of the aquatic plant Batrachium bungei along an altitudinal gradient on the Qinghai–Tibet plateau. Plant Mol Biol 111, 275–290 (2023). https://doi.org/10.1007/s11103-022-01326-0
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DOI: https://doi.org/10.1007/s11103-022-01326-0