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Comparative transcriptome analysis reveals lineage- and environment-specific adaptations in cacti from the Brazilian Atlantic Forest

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Abstract

Main conclusion

Natural selection influenced adaptive divergence between Cereus fernambucensis and Cereus insularis, revealing key genes governing abiotic stress responses and supporting neoteny in C. insularis.

Abstract

Uncovering the molecular mechanisms driving adaptive divergence in traits related to habitat adaptation remains a central challenge. In this study, we focused on the cactus clade, which includes Cereus sericifer F.Ritter, Cereus fernambucensis Lem., and Cereus insularis Hemsley. These allopatric species inhabit distinct relatively drier regions within the Brazilian Atlantic Forest, each facing unique abiotic conditions. We leveraged whole transcriptome data and abiotic variables datasets to explore lineage-specific and environment-specific adaptations in these species. Employing comparative phylogenetic methods, we identified genes under positive selection (PSG) and examined their association with non-synonymous genetic variants and abiotic attributes through a PhyloGWAS approach. Our analysis unveiled signatures of selection in all studied lineages, with C. fernambucensis northern populations and C. insularis showing the most PSGs. These PSGs predominantly govern abiotic stress regulation, encompassing heat tolerance, UV stress response, and soil salinity adaptation. Our exclusive observation of gene expression tied to early developmental stages in C. insularis supports the hypothesis of neoteny in this species. We also identified genes associated with abiotic variables in independent lineages, suggesting their role as environmental filters on genetic diversity. Overall, our findings suggest that natural selection played a pivotal role in the geographic range of these species in response to environmental and biogeographic transitions.

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Data availability

The datasets generated and analyzed in the present study are accessible through the NCBI repository under project number PRJNA1023027.

Abbreviations

BAF:

Brazilian Atlantic Forest

FNI:

Fernando de Noronha Island

GO:

Gene Ontology

GWAS:

Genome-Wide Association Studies

PSG:

Positively selected gene

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Acknowledgements

We acknowledge Gerardus Olsthoorn for his support in the sampling of plant material. We acknowledge the support of São Paulo Research Foundation (FAPESP; 2018/03428-5 to F.F.F and E.M.M; 2020/15161-3 to F.F.F; and 2022/09910-9 to D.T.A.) and National Council for Scientific and Technological Development (CNPq) (402209/2016-8 to F.F.F., 310962/2022-6 to E.M.M. and 304178/2021-7 to D.C.Z.). We also thank the fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES, Finance Code 001) to D.T.A, and FAPESP to M.R.B and M.C.T (2018/06937-8 and 2019/11233-2). We also extend our gratitude to the Fernando de Noronha Marine National Park (ICMBIO/PARNAMAR) and the government administration of Fernando de Noronha (DEFN) for their assistance in sampling Cereus insularis.

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Authors and Affiliations

  1. Centro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Santo André, São Paulo, Brazil

    Danilo T. Amaral

  2. Departamento de Ecologia e Biologia Evolutiva, Instituto de Ciências Ambientais, Químicas e Farmacêuticas, Universidade Federal de São Paulo, Diadema, São Paulo, Brazil

    Isabel A. S. Bonatelli

  3. Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611, USA

    Monique Romeiro-Brito

  4. Departamento de Biologia, Centro de Ciências Humanas e Biológicas, Universidade Federal de São Carlos (UFSCar), Rodovia João Leme dos Santos, Km 110, SP 264, Sorocaba, 18052-780, Brazil

    Milena C. Telhe, Evandro M. Moraes, Nigel Paul Taylor & Fernando F. Franco

  5. Programa de Pós-Graduação em Botânica, Instituto de Ciências Biológicas, Universidade de Brasília (UNB), Brasília, Brazil

    Daniela Cristina Zappi

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Contributions

The idea for this study was conceived by FFF and DTA. Data collection and analyses were performed by DTA, MRB, and MCT. DTA led the writing of the paper, while FFF, IASB, EMM, NT, and DZ contributed with numerous conceptions and writing. All the authors contributed to the intellectual development of the paper, made multiple revisions, and approved the final draft.

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Correspondence to Fernando F. Franco.

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Amaral, D.T., Bonatelli, I.A.S., Romeiro-Brito, M. et al. Comparative transcriptome analysis reveals lineage- and environment-specific adaptations in cacti from the Brazilian Atlantic Forest. Planta 260, 4 (2024). https://doi.org/10.1007/s00425-024-04442-x

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