Local cryptic diversity in salinity adaptation mechanisms in the wild outcrossing Brassica fruticulosa
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
679056
EC | H2020 | PRIORITY 'Excellent science' | H2020 European Research Council (ERC)
BB/P013511/1
UKRI | Biotechnology and Biological Sciences Research Council (BBSRC)
BB/R017174/1
UKRI | Biotechnology and Biological Sciences Research Council (BBSRC)
PID2019-10400RB-I00
Spanish Ministry of Science and Innovation
PubMed
39316046
PubMed Central
PMC11459175
DOI
10.1073/pnas.2407821121
Knihovny.cz E-zdroje
- Klíčová slova
- Brassicaceae, adaptation, evolution, population genomics, salinity,
- MeSH
- Brassica * genetika fyziologie metabolismus MeSH
- ekosystém MeSH
- fyziologická adaptace * genetika MeSH
- genetická variace MeSH
- genom rostlinný MeSH
- regulace genové exprese u rostlin MeSH
- salinita * MeSH
- sodík metabolismus MeSH
- tolerance k soli genetika MeSH
- transkriptom MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- sodík MeSH
It is normally supposed that populations of the same species should evolve shared mechanisms of adaptation to common stressors due to evolutionary constraint. Here, we describe a system of within-species local adaptation to coastal habitats, Brassica fruticulosa, and detail surprising strategic variability in adaptive responses to high salinity. These different adaptive responses in neighboring populations are evidenced by transcriptomes, diverse physiological outputs, and distinct genomic selective landscapes. In response to high salinity Northern Catalonian populations restrict root-to-shoot Na+ transport, favoring K+ uptake. Contrastingly, Central Catalonian populations accumulate Na+ in leaves and compensate for the osmotic imbalance with compatible solutes such as proline. Despite contrasting responses, both metapopulations were salinity tolerant relative to all inland accessions. To characterize the genomic basis of these divergent adaptive strategies in an otherwise non-saline-tolerant species, we generate a long-read-based genome and population sequencing of 18 populations (nine inland, nine coastal) across the B. fruticulosa species range. Results of genomic and transcriptomic approaches support the physiological observations of distinct underlying mechanisms of adaptation to high salinity and reveal potential genetic targets of these two very recently evolved salinity adaptations. We therefore provide a model of within-species salinity adaptation and reveal cryptic variation in neighboring plant populations in the mechanisms of adaptation to an important natural stressor highly relevant to agriculture.
Department of Botany Faculty of Science Charles University Prague 128 01 Czech Republic
Department of Plant Physiology Universitat Autònoma de Barcelona Barcelona 08193 Spain
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Zimova M., et al. , Function and underlying mechanisms of seasonal colour moulting in mammals and birds: What keeps them changing in a warming world? Biol. Rev. 93, 1478–1498 (2018). PubMed
Orteu A., Jiggins C. D., The genomics of coloration provides insights into adaptive evolution. Nat. Rev. Genet. 21, 461–475 (2020). PubMed
Magalhaes S., et al. , Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations. Nat. Ecol. Evol. 5, 251–261 (2021). PubMed PMC
Arnold B. J., et al. , Borrowed alleles and convergence in serpentine adaptation. Proc. Natl. Acad. Sci. U.S.A. 113, 8320–8325 (2016). PubMed PMC
Bohutínská M., et al. , Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives. Proc. Natl. Acad. Sci. U.S.A. 118, e2022713118 (2021). PubMed PMC
Losos J., Improbable Destinies: How Predictable is Evolution? (Penguin UK, 2017).
James M. E., Brodribb T., Wright I. J., Rieseberg L. H., Ortiz-Barrientos D., Replicated evolution in plants. Annu. Rev. Plant Biol. 74, 697–725 (2023). PubMed
Bolnick D. I., Barrett R. D., Oke K. B., Rennison D. J., Stuart Y. E., (Non) parallel evolution. Annu. Rev. Ecol. Evol. Syst. 49, 303–330 (2018).
Busoms S., et al. , Fluctuating selection on migrant adaptive sodium transporter alleles in coastal Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 115, E12443–E12452 (2018). PubMed PMC
Busoms S., Terés J., Yant L., Poschenrieder C., Salt D. E., Adaptation to coastal soils through pleiotropic boosting of ion and stress hormone concentrations in wild Arabidopsis thaliana. New Phytol. 232, 208–220 (2021). PubMed PMC
Busoms S., et al. , Salinity is an agent of divergent selection driving local adaptation of Arabidopsis to coastal habitats. Plant Physiol. 168, 915–929 (2015). PubMed PMC
Busoms S., Fisher S., Yant L., Chasing the mechanisms of ecologically adaptive salinity tolerance. Plant Commun. 4, 100571 (2023). PubMed PMC
Lynch M., et al. , Genetic drift, selection and the evolution of the mutation rate. Nat. Rev. Genet. 17, 704–714 (2016). PubMed
Yant L., Bomblies K., Genomic studies of adaptive evolution in outcrossing Arabidopsis species. Curr. Opin. Plant Biol. 36, 9–14 (2017). PubMed
Wright S. I., Ness R. W., Foxe J. P., Barrett S. C., Genomic consequences of outcrossing and selfing in plants. Int. J. Plant Sci. 169, 105–118 (2008).
Jabeen N., “Agricultural, economic and societal importance of Brassicaceae plants” in The Plant Family Brassicaceae: Biology and Physiological Responses to Environmental Stresses. Hassanuzzaman M., Ed.; Springer: Singapore, 45–128 (2020).
Quesada-Martinez D., Addo Nyarko C. P., Schiessl S. V., Mason A. S., Using wild relatives and related species to build climate resilience in Brassica crops. Theor. Appl. Genet. 134, 1711–1728 (2021). PubMed PMC
Govaerts R., Nic Lughadha E., Black N., Turner R., Paton A., The world checklist of vascular plants, a continuously updated resource for exploring global plant diversity. Sci. Data 8, 215 (2021). PubMed PMC
Chandra A., Gupta M. L., Banga S. S., Banga S. K., Production of an interspecific hybrid between Brassica fruticulosa and B. rapa. Plant Breed. 123, 497–498 (2004).
Kumar A., Singh B. K., Singh V. V., Chauhan J. S., Cytomorphological and molecular evidences of synthesis of interspecific hybrids between “Brassica rapa” and “B. fruticulosa” through sexual hybridization. Aust. J. Crop Sci. 7, 849–854 (2013).
Peñuelas J., Filella I., Sabate S., Gracia C., “Natural systems: Terrestrial ecosystems” in Report on Climate Change in Catalonia, Llebot J. E., Ed. (Institut d’Estudis Catalans; Barcelona, Spain, 2005), pp. 517–553.
Casadesús A., Bouchikh R., Munné-Bosch S., Contrasting seasonal abiotic stress and herbivory incidence in Cistus albidus L. plants growing in their natural habitat on a Mediterranean mountain. J. Arid Environ. 206, 104842 (2022).
Pérez-Martín L., et al. , Evolution of salt tolerance in Arabidopsis thaliana on siliceous soils does not confer tolerance to saline calcareous soils. Plant Soil 476, 455–475 (2022).
Hancock A. M., et al. , Adaptation to climate across the Arabidopsis thaliana genome. Science 334, 83–86 (2011). PubMed
Méndez-Vigo B., Picó F. X., Ramiro M., Martínez-Zapater J. M., Alonso-Blanco C., Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC and PHYC genes in Arabidopsis. Plant Physiol. 157, 1942–1955 (2011). PubMed PMC
Terés J., et al. , Soil carbonate drives local adaptation in Arabidopsis thaliana. Plant Cell Environ. 42, 2384–2398 (2019). PubMed PMC
Munns R., Tester M., Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681 (2008). PubMed
Simão F. A., Waterhouse R. M., Ioannidis P., Kriventseva E. V., Zdobnov E. M., BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015). PubMed
Brůna T., Hoff K. J., Lomsadze A., Stanke M., Borodovsky M., BRAKER2: Automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom. Bioinform. 3, p.lqaa108 (2021). PubMed PMC
Raj A., Stephens M., Pritchard J. K., fastSTRUCTURE: Variational inference of population structure in large SNP data sets. Genetics 197, 573–589 (2014). PubMed PMC
Skotte L., Korneliussen T. S., Albrechtsen A., Estimating individual admixture proportions from next generation sequencing data. Genetics 195, 693–702 (2013). PubMed PMC
Jombart T., adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008). PubMed
Terhorst J., Kamm J. A., Song Y. S., Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017). PubMed PMC
Médail F., Diadema K., Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J. Biogeogr. 36, 1333–1345 (2009).
Almeida P., Katschnig D., De Boer A. H., HKT transporters—State of the art. Int. J. Mol. Sci. 14, 20359–20385 (2013). PubMed PMC
Chu M., Chen P., Meng S., Xu P., Lan W., The Arabidopsis phosphatase PP2C49 negatively regulates salt tolerance through inhibition of AtHKT1; 1. J. Integr. Plant Biol. 63, 528–542 (2021). PubMed
Nieves-Cordones M., Alemán F., Martínez V., Rubio F., The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol. Plant 3, 326–333 (2010). PubMed
Qiu Q. S., Guo Y., Dietrich M. A., Schumaker K. S., Zhu J. K., Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U.S.A. 99, 8436–8441 (2002). PubMed PMC
Shi H., Lee B. H., Wu S. J., Zhu J. K., Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat. Biotechnol. 21, 81–85 (2003). PubMed
Kumar G., Purty R. S., Sharma M. P., Singla-Pareek S. L., Pareek A., Physiological responses among Brassica species under salinity stress show strong correlation with transcript abundance for SOS pathway-related genes. J. Plant Physiol. 166, 507–520 (2009). PubMed
Hasegawa P. M., Sodium (Na+) homeostasis and salt tolerance of plants Environ. Exp. Bot. 92, 19–31 (2013).
Ye C., Yang X., Xia X., Yin W., Comparative analysis of cation/proton antiporter superfamily in plants. Gene 521, 245–251 (2013). PubMed
Guo Y., Zhu C., Tian Z., Overexpression of KvCHX enhances salt tolerance in Arabidopsis thaliana seedlings. Curr. Issues Mol. Biol. 45, 9692–9708 (2023). PubMed PMC
Zhao S., et al. , Regulation of plant responses to salt stress. Int. J. Mol. Sci. 22, 4609 (2021). PubMed PMC
Choi W. G., Toyota M., Kim S. H., Hilleary R., Gilroy S., Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc. Natl. Acad. Sci. U.S.A. 111, 6497–6502 (2014). PubMed PMC
Funck D., Baumgarten L., Stift M., Von Wirén N., Schönemann L., Differential contribution of P5CS isoforms to stress tolerance in Arabidopsis. Front. Plant Sci. 11, 565134 (2020). PubMed PMC
Caye K., Jumentier B., Lepeule J., François O., LFMM 2: Fast and accurate inference of gene-environment associations in genome-wide studies. Mol. Biol. Evol. 36, 852–860 (2019). PubMed PMC
Luu K., Bazin E., Blum M. G., pcadapt: An R package to perform genome scans for selection based on principal component analysis. Mol. Ecol. Resour. 17, 67–77 (2017). PubMed
Gautam A., Pandey A. K., Aquaporins responses under challenging environmental conditions and abiotic stress tolerance in plants. Bot. Rev. 87, 467–495 (2021).
Kant P., Kant S., Gordon M., Shaked R., Barak S., STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol. 145, 814–830 (2007). PubMed PMC
Oh H., Dassanayake M., Landscape of gene transposition–duplication within the Brassicaceae family. DNA Res. 26, 21–36 (2019). PubMed PMC
Gao L., Xiang C. B., The genetic locus At1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance in Arabidopsis. Plant Mol. Biol. 67, 125–134 (2008). PubMed
Li P., et al. , The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J. 89, 85–103 (2017). PubMed
Yuenyong W., Sirikantaramas S., Qu L. J., Buaboocha T., Isocitrate lyase plays important roles in plant salt tolerance. BMC Plant Biol. 19, 1–14 (2019). PubMed PMC
Hesp P. A., Ecological processes and plant adaptations on coastal dunes. J. Arid Environ. 21, 165–191 (1991).
Bennett J. R., Dunwiddie P. W., Giblin D. E., Arcese P., Native versus exotic community patterns across three scales: Roles of competition, environment and incomplete invasion. Perspect. Plant Ecol. Evol. Syst. 14, 381–392 (2012).
Jain S. K., Bradshaw A. D., Evolutionary divergence among adjacent plant populations. I. The evidence and its theoretical analysis. Theor. Appl. Genet. 72, 314–321 (1966).
Irmak S., Kabenge I., Skaggs K. E., Mutiibwa D., Trend and magnitude of changes in climate variables and reference evapotranspiration over 116-yr period in the Platte River Basin, Central Nebraska–USA. J. Hydrol. 420, 228–244 (2012).
Abderrahman W. A., Bader T. A., Kahn A. U., Ajward M. H., Weather modification impact on reference evapotranspiration, soil salinity and desertification in arid regions: A case study. J. Arid Environ. 20, 277–286 (1991).
Bates L. S., Waldren R. P. A., Teare I. D., Rapid determination of free proline for water-stress studies. Plant Soil 39, 205–207 (1973).
Bernatzky R., Tanksley S. D., Genetics of actin-related sequences in tomato. Theor. Appl. Genet. 72, 314–321 (1986). PubMed
Wick R. R., Judd L. M., Holt K. E., Performance of neural network base-calling tools for Oxford Nanopore sequencing. Genome Biol. 20, 1–10 (2019). PubMed PMC
Kolmogorov M. A., Algorithms for Long-Read Assembly (University of California, San Diego, 2019).
Sun H., Ding J., Piednoël M., Schneeberger K., findGSE: Estimating genome size variation within human and Arabidopsis using k-mer frequencies. Bioinformatics 34, 550–557 (2018). PubMed
Wright C., Wykes M., Medaka. github.com/nanoporetech/medaka (2022). Accessed 22 December 2022.
Walker B. J., et al. , Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9, e112963 (2014). PubMed PMC
Guan D., et al. , Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020). PubMed PMC
Laetsch D. R., Blaxter M. L., BlobTools: Interrogation of genome assemblies. F1000Res. 6, 1287 (2017).
Buchfink B., Reuter K., Drost H. G., Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021). PubMed PMC
Manni M., Berkeley M. R., Seppey M., Zdobnov E. M., BUSCO: Assessing genomic data quality and beyond. Curr. Protoc. 1, e323 (2021). PubMed
Bolger A. M., Lohse M., Usadel B., Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). PubMed PMC
Vasimuddin M., Misra S., Li H., Aluru S., “Eficient architecture-aware acceleration of BWA-MEM for multicore systems” in 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS) (2019), pp. 314–324.
Van der Auwera G. A., O’Connor B. D., Genomics in the Cloud: Using Docker, GATK, and WDL in Terra (O’Reilly Media, 2020).
Hamala T., et al. , Impact of whole-genome duplications on structural variant evolution in the plant genus Cochlearia. Nat. Commun. 15, 5377 (2024). PubMed PMC
Patterson N., Price A. L., Reich D., Population structure and eigenanalysis. PLoS Genet 2, 1–20 (2006). PubMed PMC
Ossowski S., et al. , The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92–94 (2010). PubMed PMC
Korneliussen T. S., Albrechtsen A., Nielsen R., ANGSD: Analysis of next generation sequencing data. BMC Bioinf. 15, 1–13 (2014). PubMed PMC
Tajima F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–597 (1989). PubMed PMC
Huson D. H., Bryant D., Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267 (2006). PubMed
Nielsen R., Korneliussen T., Albrechtsen A., Li Y., Wang J., SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS One 7, e37558 (2012). PubMed PMC
Bhatia G., Patterson N., Sankararaman S., Price A. L., Estimating and interpreting FST: The impact of rare variants. Genome Res. 23, 1514–1521 (2013). PubMed PMC
Lewontin R. C., Krakauer J., Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74, 175–181 (1973). PubMed PMC
Wickham H., Chang W., Wickham M. H., Package ‘ggplot2’. Create elegant data visualisations using the grammar of graphics (Version 2, Springer, 2016), pp. 1–189.
Liao Y., Smyth G. K., Shi W., The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 47, e47 (2019). PubMed PMC
Danecek P., et al. , Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021). PubMed PMC
Anders S., Pyl P. T., Huber W., HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015). PubMed PMC
Overbey E. G., et al. , NASA GeneLab RNA-seq consensus pipeline: Standardized processing of short-read RNA-seq data. iScience 24, 102361 (2021). PubMed PMC
Emms D. M., Kelly S., OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019). PubMed PMC
Zotarelli L., Dukes M. D., Romero C. C., Migliaccio K. W., Morgan K. T., Step by step calculation of the Penman-Monteith Evapotranspiration (FAO-56 Method) AE459. (Agricultural and Biological Engineering Department, Florida Cooperative Extension Service, IFAS, UF, 2010; ), p. 12.
Busoms S., et al. , Data from “Local cryptic diversity in salinity adaptation mechanisms in the wild outcrossing Brassica fruticulosa”. Sequence data. https://www.ebi.ac.uk/ena/browser/view/PRJEB74663. Deposited 1 June 2024. PubMed PMC