IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32180-9.html
   My bibliography  Save this article

Three types of genes underlying the Gametophyte factor1 locus cause unilateral cross incompatibility in maize

Author

Listed:
  • Yuebin Wang

    (Huazhong Agricultural University)

  • Wenqiang Li

    (Huazhong Agricultural University)

  • Luxi Wang

    (Huazhong Agricultural University)

  • Jiali Yan

    (Huazhong Agricultural University)

  • Gang Lu

    (Huazhong Agricultural University)

  • Ning Yang

    (Huazhong Agricultural University
    Hubei Hongshan Laboratory)

  • Jieting Xu

    (Huazhong Agricultural University)

  • Yuqing Wang

    (Huazhong Agricultural University)

  • Songtao Gui

    (Huazhong Agricultural University)

  • Gengshen Chen

    (Huazhong Agricultural University)

  • Shuyan Li

    (Huazhong Agricultural University)

  • Chengxiu Wu

    (Huazhong Agricultural University)

  • Tingting Guo

    (Huazhong Agricultural University
    Hubei Hongshan Laboratory)

  • Yingjie Xiao

    (Huazhong Agricultural University
    Hubei Hongshan Laboratory)

  • Marilyn L. Warburton

    (USDA ARS Corn Host Plant Resistance Research Unit)

  • Alisdair R. Fernie

    (Max-Planck-Institute of Molecular Plant Physiology)

  • Thomas Dresselhaus

    (University of Regensburg)

  • Jianbing Yan

    (Huazhong Agricultural University
    Hubei Hongshan Laboratory)

Abstract

Unilateral cross incompatibility (UCI) occurs between popcorn and dent corn, and represents a critical step towards speciation. It has been reported that ZmGa1P, encoding a pectin methylesterase (PME), is a male determinant of the Ga1 locus. However, the female determinant and the genetic relationship between male and female determinants at this locus are unclear. Here, we report three different types, a total of seven linked genes underlying the Ga1 locus, which control UCI phenotype by independently affecting pollen tube growth in both antagonistic and synergistic manners. These include five pollen-expressed PME genes (ZmGa1Ps-m), a silk-expressed PME gene (ZmPME3), and another silk-expressed gene (ZmPRP3), encoding a pathogenesis-related (PR) proteins. ZmGa1Ps-m confer pollen compatibility. Presence of ZmPME3 causes silk to reject incompatible pollen. ZmPRP3 promotes incompatibility pollen tube growth and thereby breaks the blocking effect of ZmPME3. In addition, evolutionary genomics analyses suggest that the divergence of the Ga1 locus existed before maize domestication and continued during breeding improvement. The knowledge gained here deepen our understanding of the complex regulation of cross incompatibility.

Suggested Citation

  • Yuebin Wang & Wenqiang Li & Luxi Wang & Jiali Yan & Gang Lu & Ning Yang & Jieting Xu & Yuqing Wang & Songtao Gui & Gengshen Chen & Shuyan Li & Chengxiu Wu & Tingting Guo & Yingjie Xiao & Marilyn L. Wa, 2022. "Three types of genes underlying the Gametophyte factor1 locus cause unilateral cross incompatibility in maize," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32180-9
    DOI: 10.1038/s41467-022-32180-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32180-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32180-9?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. Hidenori Takeuchi & Tetsuya Higashiyama, 2016. "Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis," Nature, Nature, vol. 531(7593), pages 245-248, March.
    2. Nick Patterson & Alkes L Price & David Reich, 2006. "Population Structure and Eigenanalysis," PLOS Genetics, Public Library of Science, vol. 2(12), pages 1-20, December.
    3. Zhaogui Zhang & Baocai Zhang & Zhibin Chen & Dongmei Zhang & Huairen Zhang & Hang Wang & Yu’e Zhang & Darun Cai & Juan Liu & Senlin Xiao & Yanqing Huo & Jie Liu & Lanjun Zhang & Mingming Wang & Xu Liu, 2018. "A PECTIN METHYLESTERASE gene at the maize Ga1 locus confers male function in unilateral cross-incompatibility," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    4. Qiaohong Duan & Daniel Kita & Eric A. Johnson & Mini Aggarwal & Laura Gates & Hen-Ming Wu & Alice Y. Cheung, 2014. "Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
    5. Yongxian Lu & Samuel A. Hokin & Jerry L. Kermicle & Thomas Hartwig & Mathew M. S. Evans, 2019. "A pistil-expressed pectin methylesterase confers cross-incompatibility between strains of Zea mays," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    6. Xiaoxiao Zhang & Weijia Liu & Takuya T. Nagae & Hidenori Takeuchi & Heqiao Zhang & Zhifu Han & Tetsuya Higashiyama & Jijie Chai, 2017. "Structural basis for receptor recognition of pollen tube attraction peptides," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    Full references (including those not matched with items on IDEAS)

    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. Shimin You & Zhigang Zhao & Xiaowen Yu & Shanshan Zhu & Jian Wang & Dekun Lei & Jiawu Zhou & Jing Li & Haiyuan Chen & Yanjia Xiao & Weiwei Chen & Qiming Wang & Jiayu Lu & Keyi Chen & Chunlei Zhou & Xi, 2023. "A toxin-antidote system contributes to interspecific reproductive isolation in rice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Zhibin Chen & Zhaogui Zhang & Huairen Zhang & Kai Li & Darun Cai & Li Zhao & Juan Liu & Huabang Chen, 2022. "A pair of non-Mendelian genes at the Ga2 locus confer unilateral cross-incompatibility in maize," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Gyaneshwer Chaubey & Anurag Kadian & Saroj Bala & Vadlamudi Raghavendra Rao, 2015. "Genetic Affinity of the Bhil, Kol and Gond Mentioned in Epic Ramayana," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-11, June.
    4. Estavoyer, Maxime & François, Olivier, 2022. "Theoretical analysis of principal components in an umbrella model of intraspecific evolution," Theoretical Population Biology, Elsevier, vol. 148(C), pages 11-21.
    5. Hyosik Jang & Ian M Ehrenreich, 2012. "Genome-Wide Characterization of Genetic Variation in the Unicellular, Green Alga Chlamydomonas reinhardtii," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-9, July.
    6. Xiaofeng Cai & Xuepeng Sun & Chenxi Xu & Honghe Sun & Xiaoli Wang & Chenhui Ge & Zhonghua Zhang & Quanxi Wang & Zhangjun Fei & Chen Jiao & Quanhua Wang, 2021. "Genomic analyses provide insights into spinach domestication and the genetic basis of agronomic traits," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Lee, Anthony J. & Hibbs, Courtney & Wright, Margaret J. & Martin, Nicholas G. & Keller, Matthew C. & Zietsch, Brendan P., 2017. "Assessing the accuracy of perceptions of intelligence based on heritable facial features," Intelligence, Elsevier, vol. 64(C), pages 1-8.
    8. Thompson Katherine L. & Linnen Catherine R. & Kubatko Laura, 2016. "Tree-based quantitative trait mapping in the presence of external covariates," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 15(6), pages 473-490, December.
    9. Jacobo Pardo-Seco & Alberto Gómez-Carballa & Jorge Amigo & Federico Martinón-Torres & Antonio Salas, 2014. "A Genome-Wide Study of Modern-Day Tuscans: Revisiting Herodotus's Theory on the Origin of the Etruscans," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-11, September.
    10. Ilja M Nolte & Chris Wallace & Stephen J Newhouse & Daryl Waggott & Jingyuan Fu & Nicole Soranzo & Rhian Gwilliam & Panos Deloukas & Irina Savelieva & Dongling Zheng & Chrysoula Dalageorgou & Martin F, 2009. "Common Genetic Variation Near the Phospholamban Gene Is Associated with Cardiac Repolarisation: Meta-Analysis of Three Genome-Wide Association Studies," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-10, July.
    11. Hoicheong Siu & Li Jin & Momiao Xiong, 2012. "Manifold Learning for Human Population Structure Studies," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-18, January.
    12. Elodie Persyn & Richard Redon & Lise Bellanger & Christian Dina, 2018. "The impact of a fine-scale population stratification on rare variant association test results," PLOS ONE, Public Library of Science, vol. 13(12), pages 1-17, December.
    13. Andre Krumel Portella & Afroditi Papantoni & Catherine Paquet & Spencer Moore & Keri Shiels Rosch & Stewart Mostofsky & Richard S Lee & Kimberly R Smith & Robert Levitan & Patricia Pelufo Silveira & S, 2020. "Predicted DRD4 prefrontal gene expression moderates snack intake and stress perception in response to the environment in adolescents," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-20, June.
    14. Lindsay Fernández-Rhodes & Jennifer R Malinowski & Yujie Wang & Ran Tao & Nathan Pankratz & Janina M Jeff & Sachiko Yoneyama & Cara L Carty & V Wendy Setiawan & Loic Le Marchand & Christopher Haiman &, 2018. "The genetic underpinnings of variation in ages at menarche and natural menopause among women from the multi-ethnic Population Architecture using Genomics and Epidemiology (PAGE) Study: A trans-ethnic ," PLOS ONE, Public Library of Science, vol. 13(7), pages 1-21, July.
    15. Peña-Malavera Andrea & Bruno Cecilia & Balzarini Monica & Fernandez Elmer, 2014. "Comparison of algorithms to infer genetic population structure from unlinked molecular markers," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 13(4), pages 1-12, August.
    16. Chi-Chun Liu & David Witonsky & Anna Gosling & Ju Hyeon Lee & Harald Ringbauer & Richard Hagan & Nisha Patel & Raphaela Stahl & John Novembre & Mark Aldenderfer & Christina Warinner & Anna Di Rienzo &, 2022. "Ancient genomes from the Himalayas illuminate the genetic history of Tibetans and their Tibeto-Burman speaking neighbors," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Gad Abraham & Michael Inouye, 2014. "Fast Principal Component Analysis of Large-Scale Genome-Wide Data," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-5, April.
    18. Zhao Huaqing & Rebbeck Timothy R. & Mitra Nandita, 2012. "Analyzing Genetic Association Studies with an Extended Propensity Score Approach," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(5), pages 1-24, October.
    19. Diana Chang & Alon Keinan, 2014. "Principal Component Analysis Characterizes Shared Pathogenetics from Genome-Wide Association Studies," PLOS Computational Biology, Public Library of Science, vol. 10(9), pages 1-14, September.
    20. Emile R Chimusa & Michelle Daya & Marlo Möller & Raj Ramesar & Brenna M Henn & Paul D van Helden & Nicola J Mulder & Eileen G Hoal, 2013. "Determining Ancestry Proportions in Complex Admixture Scenarios in South Africa Using a Novel Proxy Ancestry Selection Method," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-14, September.

    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:13:y:2022:i:1:d:10.1038_s41467-022-32180-9. 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.