IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51032-2.html
   My bibliography  Save this article

Adaptive gene loss in the common bean pan-genome during range expansion and domestication

Author

Listed:
  • Gaia Cortinovis

    (Marche Polytechnic University)

  • Leonardo Vincenzi

    (University of Verona)

  • Robyn Anderson

    (University of Western Australia)

  • Giovanni Marturano

    (University of Verona)

  • Jacob Ian Marsh

    (University of Western Australia)

  • Philipp Emanuel Bayer

    (University of Western Australia)

  • Lorenzo Rocchetti

    (Marche Polytechnic University)

  • Giulia Frascarelli

    (Marche Polytechnic University)

  • Giovanna Lanzavecchia

    (Marche Polytechnic University)

  • Alice Pieri

    (Marche Polytechnic University)

  • Andrea Benazzo

    (University of Ferrara)

  • Elisa Bellucci

    (Marche Polytechnic University)

  • Valerio Vittori

    (Marche Polytechnic University)

  • Laura Nanni

    (Marche Polytechnic University)

  • Juan José Ferreira Fernández

    (Ctra AS-267 PK 19)

  • Marzia Rossato

    (University of Verona
    Genartis s.r.l)

  • Orlando Mario Aguilar

    (CCT La Plata)

  • Peter Laurent Morrell

    (University of Minnesota)

  • Monica Rodriguez

    (University of Sassari
    CBV—Centro per la Conservazione e Valorizzazione della Biodiversità Vegetale, University of Sassari)

  • Tania Gioia

    (University of Basilicata)

  • Kerstin Neumann

    (Leibniz Institute of Plant Genetics and Crop Plant Research (IPK))

  • Juan Camilo Alvarez Diaz

    (University Paris-Saclay)

  • Ariane Gratias

    (University Paris-Saclay)

  • Christophe Klopp

    (Sigenae, MIAT)

  • Elena Bitocchi

    (Marche Polytechnic University)

  • Valérie Geffroy

    (University Paris-Saclay)

  • Massimo Delledonne

    (University of Verona
    Genartis s.r.l)

  • David Edwards

    (University of Western Australia)

  • Roberto Papa

    (Marche Polytechnic University)

Abstract

The common bean (Phaseolus vulgaris L.) is a crucial legume crop and an ideal evolutionary model to study adaptive diversity in wild and domesticated populations. Here, we present a common bean pan-genome based on five high-quality genomes and whole-genome reads representing 339 genotypes. It reveals ~234 Mb of additional sequences containing 6,905 protein-coding genes missing from the reference, constituting 49% of all presence/absence variants (PAVs). More non-synonymous mutations are found in PAVs than core genes, probably reflecting the lower effective population size of PAVs and fitness advantages due to the purging effect of gene loss. Our results suggest pan-genome shrinkage occurred during wild range expansion. Selection signatures provide evidence that partial or complete gene loss was a key adaptive genetic change in common bean populations with major implications for plant adaptation. The pan-genome is a valuable resource for food legume research and breeding for climate change mitigation and sustainable agriculture.

Suggested Citation

  • Gaia Cortinovis & Leonardo Vincenzi & Robyn Anderson & Giovanni Marturano & Jacob Ian Marsh & Philipp Emanuel Bayer & Lorenzo Rocchetti & Giulia Frascarelli & Giovanna Lanzavecchia & Alice Pieri & And, 2024. "Adaptive gene loss in the common bean pan-genome during range expansion and domestication," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51032-2
    DOI: 10.1038/s41467-024-51032-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51032-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51032-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Landgraf, Andrew J. & Lee, Yoonkyung, 2020. "Dimensionality reduction for binary data through the projection of natural parameters," Journal of Multivariate Analysis, Elsevier, vol. 180(C).
    2. Xiaolei Liu & Meng Huang & Bin Fan & Edward S Buckler & Zhiwu Zhang, 2016. "Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome-Wide Association Studies," PLOS Genetics, Public Library of Science, vol. 12(2), pages 1-24, February.
    3. Dieter Gerten & Vera Heck & Jonas Jägermeyr & Benjamin Leon Bodirsky & Ingo Fetzer & Mika Jalava & Matti Kummu & Wolfgang Lucht & Johan Rockström & Sibyll Schaphoff & Hans Joachim Schellnhuber, 2020. "Feeding ten billion people is possible within four terrestrial planetary boundaries," Nature Sustainability, Nature, vol. 3(3), pages 200-208, March.
    4. Murukarthick Jayakodi & Sudharsan Padmarasu & Georg Haberer & Venkata Suresh Bonthala & Heidrun Gundlach & Cécile Monat & Thomas Lux & Nadia Kamal & Daniel Lang & Axel Himmelbach & Jennifer Ens & Xiao, 2020. "The barley pan-genome reveals the hidden legacy of mutation breeding," Nature, Nature, vol. 588(7837), pages 284-289, December.
    5. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Haifei Hu & Junliang Zhao & William J. W. Thomas & Jacqueline Batley & David Edwards, 2025. "The role of pangenomics in orphan crop improvement," Nature Communications, Nature, vol. 16(1), pages 1-9, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hikaru Hayashi & Sayaka Seki & Takeshi Tomita & Masayoshi Kato & Norihiro Ashihara & Tokuhiro Chano & Hideki Sanjo & Miwa Kawade & Chenhui Yan & Hiroki Sakai & Hidenori Tomida & Miyuki Tanaka & Mai Iw, 2025. "Synthetic short mRNA prevents metastasis via innate-adaptive immunity," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    2. Xiangwei Li & Thomas Delerue & Ben Schöttker & Bernd Holleczek & Eva Grill & Annette Peters & Melanie Waldenberger & Barbara Thorand & Hermann Brenner, 2022. "Derivation and validation of an epigenetic frailty risk score in population-based cohorts of older adults," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Ethan Gordon & Federico Davila & Chris Riedy, 2022. "Transforming landscapes and mindscapes through regenerative agriculture," Agriculture and Human Values, Springer;The Agriculture, Food, & Human Values Society (AFHVS), vol. 39(2), pages 809-826, June.
    5. Hao A. Duong & Kenkichi Baba & Jason P. DeBruyne & Alec J. Davidson & Christopher Ehlen & Michael Powell & Gianluca Tosini, 2024. "Environmental circadian disruption re-writes liver circadian proteomes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Ma, Shuai & Wang, Liang-Jie & Chu, Lei & Jiang, Jiang, 2023. "Determination of ecological restoration patterns based on water security and food security in arid regions," Agricultural Water Management, Elsevier, vol. 278(C).
    7. Ramachandran Prakasam & Angela Bonadiman & Roberta Andreotti & Emanuela Zuccaro & Davide Dalfovo & Caterina Marchioretti & Debasmita Tripathy & Gianluca Petris & Eric N. Anderson & Alice Migazzi & Lau, 2023. "LSD1/PRMT6-targeting gene therapy to attenuate androgen receptor toxic gain-of-function ameliorates spinobulbar muscular atrophy phenotypes in flies and mice," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    8. Li Guo & Cheng Hu & Yang Liu & Xiaoyu Chen & Deli Song & Runling Shen & Zhanzhen Liu & Xudong Jia & Qinfen Zhang & Yuanzhu Gao & Zhezhi Deng & Tao Zuo & Jun Hu & Wenbo Zhu & Jing Cai & Guangmei Yan & , 2023. "Directed natural evolution generates a next-generation oncolytic virus with a high potency and safety profile," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    10. Tianshi Feng & Xuemei Zhao & Ping Gu & Wah Yang & Cunchuan Wang & Qingyu Guo & Qiaoyun Long & Qing Liu & Ying Cheng & Jin Li & Cynthia Kwan Yui Cheung & Donghai Wu & Xinyu Kong & Yong Xu & Dewei Ye & , 2022. "Adipocyte-derived lactate is a signalling metabolite that potentiates adipose macrophage inflammation via targeting PHD2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Elisa Bellucci & Andrea Benazzo & Chunming Xu & Elena Bitocchi & Monica Rodriguez & Saleh Alseekh & Valerio Di Vittori & Tania Gioia & Kerstin Neumann & Gaia Cortinovis & Giulia Frascarelli & Ester Mu, 2023. "Selection and adaptive introgression guided the complex evolutionary history of the European common bean," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Jiayin Peng & Lili Han & Biao Liu & Jiawen Song & Yuang Wang & Kunpeng Wang & Qian Guo & XinYan Liu & Yu Li & Jujin Zhang & Wenqing Wu & Sheng Li & Xin Fu & Cheng-le Zhuang & Weikang Zhang & Shengbao , 2023. "Gli1 marks a sentinel muscle stem cell population for muscle regeneration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Xiaolin Yang & Jinran Xiong & Taisheng Du & Xiaotang Ju & Yantai Gan & Sien Li & Longlong Xia & Yanjun Shen & Steven Pacenka & Tammo S. Steenhuis & Kadambot H. M. Siddique & Shaozhong Kang & Klaus But, 2024. "Diversifying crop rotation increases food production, reduces net greenhouse gas emissions and improves soil health," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Brent S. Perlman & Noah Burget & Yeqiao Zhou & Gregory W. Schwartz & Jelena Petrovic & Zora Modrusan & Robert B. Faryabi, 2024. "Enhancer-promoter hubs organize transcriptional networks promoting oncogenesis and drug resistance," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    15. Elisa Setten & Alessandra Castagna & Josué Manik Nava-Sedeño & Jonathan Weber & Roberta Carriero & Andreas Reppas & Valery Volk & Jessica Schmitz & Wilfried Gwinner & Haralampos Hatzikirou & Friedrich, 2022. "Understanding fibrosis pathogenesis via modeling macrophage-fibroblast interplay in immune-metabolic context," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    16. Guangbao Guo & Guoqi Qian & Lu Lin & Wei Shao, 2021. "Parallel inference for big data with the group Bayesian method," Metrika: International Journal for Theoretical and Applied Statistics, Springer, vol. 84(2), pages 225-243, February.
    17. Andrea Zanetti & Gwendal Dujardin & Lucas Fares-Taie & Jeanne Amiel & Jérôme E. Roger & Isabelle Audo & Matthieu P. Robert & Pierre David & Vincent Jung & Nicolas Goudin & Ida Chiara Guerrera & Stépha, 2024. "GPATCH11 variants cause mis-splicing and early-onset retinal dystrophy with neurological impairment," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    18. Ebun Akinsete & Alina Velias & Phoebe Koundouri, 2023. "Integrating Experimental Economics and Living Labs In Water Resource Management," DEOS Working Papers 2301, Athens University of Economics and Business.
    19. Dafne Ibarra-Morales & Michael Rauer & Piergiuseppe Quarato & Leily Rabbani & Fides Zenk & Mariana Schulte-Sasse & Francesco Cardamone & Alejandro Gomez-Auli & Germano Cecere & Nicola Iovino, 2021. "Histone variant H2A.Z regulates zygotic genome activation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    20. María Elena Murrieta-Oquendo & Iván Manuel De la Vega, 2022. "State and Dynamics of the Innovative Performance of Medium and Large Firms in the Manufacturing Sector in Emerging Economies: The Cases of Peru and Ecuador," Sustainability, MDPI, vol. 15(1), pages 1-23, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51032-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.