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Cited by 1Chromosomal and Genetic VariationsPlant Reproductive BiologyGenetic Mapping and Diversity in Plants and Animals

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Molecular evolution of a reproductive barrier in maize and related species

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Cryan, Elli, Phinney, Garnet, Seetharam, Arun S, Evans, Matthew M S, Kellogg, Elizabeth A, Zhan, Junpeng, Meyers, Blake, Kliebenstein, Daniel J, Ross-Ibarra, Jeffrey·2025·GENETICS
DOI 10.1093/genetics/iyaf085PMC PMC12239200

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Abstract

Three cross-incompatibility loci each control a distinct reproductive barrier in both domesticated maize (Zea mays ssp. mays) and its wild teosinte relatives. These 3 loci, Teosinte crossing barrier1 (Tcb1), Gametophytic factor1 (Ga1), and Ga2, each play a key role in preventing hybridization between incompatible populations and are proposed to maintain the barrier between domesticated and wild subspecies. Each locus encodes both a silk-active and a matching pollen-active pectin methylesterase (PMEs). To investigate the diversity and molecular evolution of these gametophytic factor loci, we identified existing and improved models of the responsible genes in a new genome assembly of maize line P8860 that contains active versions of all 3 loci. We then examined 52 assembled genomes from 17 species to classify haplotype diversity and identify sites under diversifying selection during the evolution of these genes. We show that Ga2, the oldest of these 3 loci, was duplicated to form Ga1 at least 12 million years ago. Tcb1, the youngest locus, arose as a duplicate of Ga1 before or around the time of diversification of the Zea genus. We find evidence of positive selection during evolution of the functional genes at an active site in the pollen-expressed PME and predicted surface sites in both the silk- and pollen-expressed PMEs. The most common allele at the Ga1 locus is a conserved ga1 allele (ga1-Off), which is specific haplotype containing 3 full-length PME gene copies, all of which are noncoding due to conserved stop codons and are between 610 thousand and 1.5 million years old. We show that the ga1-Off allele is associated with and likely generates 24-nt siRNAs in developing pollen-producing tissue, and these siRNAs map to functional Ga1 alleles. In previously published crosses, the ga1-Off allele was associated with reduced function of the typically dominant functional alleles for the Ga1 and Tcb1 barriers. Taken together, this seems to be an example of an allele at a reproductive barrier locus being associated with an as yet undetermined mechanism capable of silencing the reproductive barrier.

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Research works printed but not linked: 78

  1. Almagro Armenteros, 2019, Detecting sequence signals in targeting peptides using deep learning, Life Sci Alliance., 2, e201900429, 10.26508/lsa.201900429 · DOI
  2. Ashman, 1975, Modification of cross-sterility in maize, J Hered., 66, 5, 10.1093/oxfordjournals.jhered.a108577 · DOI
  3. Baack, 2015, The origins of reproductive isolation in plants, New Phytol., 207, 968, 10.1111/nph.13424 · DOI · Paper page
  4. Bapat, 2023, The ga1 locus of the genus Zea is associated with novel genome structures derived from multiple, independent nonhomologous recombination events, G3 (Bethesda), 13, jkad196, 10.1093/g3journal/jkad196 · DOI
  5. Begcy, 2024, Maize stigmas react differently to self- and cross-pollination and fungal invasion, Plant Physiol., 196, 3071, 10.1093/plphys/kiae536 · DOI
  6. Berube B, Ernst E, Cahn J, Roche B, de Santis Alves C, Lynn J, Scheben A, Grimanelli D, Siepel A, Ross-Ibarra J, et al., 2024, 10.1038/s41586-024-07788-0 · DOI
  7. Brieger, 1937, Genetic control of gametophyte development in maize: I. A gametophyte character in chromosome five, J Genet., 34, 57, 10.1007/BF02982255 · DOI
  8. Broz, 2021, Pollen-pistil interactions as reproductive barriers, Annu Rev Plant Biol., 72, 615, 10.1146/annurev-arplant-080620-102159 · DOI
  9. Bukowski, 2018, Construction of the third-generation Zea mays haplotype map, GigaScience, 7, 1, 10.1093/gigascience/gix134 · DOI
  10. Burnham, 1936, Differential fertilization in the Bt Pr linkage group of maize1, Agron J., 28, 968, 10.2134/agronj1936.00021962002800120002x · DOI
  11. Chen, 2022, A pair of non-Mendelian genes at the ga2 locus confer unilateral cross-incompatibility in maize, Nat Commun., 13, 1993, 10.1038/s41467-022-29729-z · DOI
  12. Cheng, 2021, Haplotype-resolved de novo assembly using phased assembly graphs with Hifiasm, Nat Methods., 18, 170, 10.1038/s41592-020-01056-5 · DOI · Paper page
  13. Chow, 2023, Small RNA-mediated DNA methylation during plant reproduction, Plant Cell., 35, 1787, 10.1093/plcell/koad010 · DOI
  14. Christie, 2022, The strength of reproductive isolating barriers in seed plants: insights from studies quantifying premating and postmating reproductive barriers over the past 15 years, Evolution., 76, 2228, 10.1111/evo.14565 · DOI
  15. Clark, 2005, Estimating a nucleotide substitution rate for maize from polymorphism at a Major domestication locus, Mol Biol Evol., 22, 2304, 10.1093/molbev/msi228 · DOI
  16. Correns, 1901, Bastarde Zwischen Maisrassem, mit Besonderer Berücksichtigung Der Xenien, Bibl. Bot, 10
  17. Davidson, 2012, Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution: comparative transcriptome analyses in grasses, Plant J., 71, 492, 10.1111/j.1365-313X.2012.05005.x · DOI
  18. Demerec, 1929, Cross sterility in maize, Mol Genet Genomics., 50, 281, 10.1007/BF01742059 · DOI
  19. Di Matteo, 2005, Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein, Plant Cell., 17, 849, 10.1105/tpc.104.028886 · DOI
  20. Dresselhaus, 2011, Using maize as a model to study pollen tube growth and guidance, cross-incompatibility and sperm delivery in grasses, Ann Bot., 108, 727, 10.1093/aob/mcr017 · DOI
  21. Edgar, 2022, Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny, Nat Commun., 13, 6968, 10.1038/s41467-022-34630-w · DOI
  22. Evans, 2001, Teosinte crossing barrier1, a locus governing hybridization of teosinte with maize, Theor Appl Genet., 103, 259, 10.1007/s001220100549 · DOI
  23. Flint-Garcia, 2005, Maize association population: a high-resolution platform for quantitative trait locus dissection: high-resolution maize association population, Plant J., 44, 1054, 10.1111/j.1365-313X.2005.02591.x · DOI
  24. Fryxell, 1996, The coevolution of gene family trees, Trends Genet., 12, 364, 10.1016/S0168-9525(96)80020-5 · DOI
  25. Goodman, 2021, Maize cross incompatibility and the promiscuous Ga1-m allele, Plant Breed Rev., 44, 31, 10.1002/9781119717003.ch2 · DOI
  26. Grass Phylogeny Working Group III, 2025, A nuclear phylogenomic tree of grasses (Poaceae) recovers current classification despite gene tree incongruence, New Phytol., 245, 818, 10.1111/nph.20263 · DOI
  27. Hufford, 2021, De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes, Science (New York, N.Y.), 373, 655, 10.1126/science.abg5289 · DOI · Paper page
  28. Johansson, 2002, Crystal structure of plant pectin methylesterase, FEBS Lett., 514, 243, 10.1016/S0014-5793(02)02372-4 · DOI
  29. Kermicle, 2006, A selfish gene governing pollen-pistil compatibility confers reproductive isolation between maize relatives, Genetics, 172, 499, 10.1534/genetics.105.048645 · DOI
  30. Kermicle, 1990, Cross-incompatibility between maize and teosinte, Maydica, 35, 399
  31. Kermicle, 2005, Pollen–pistil barriers to crossing in maize and teosinte result from incongruity rather than active rejection, Sex Plant Reprod., 18, 187, 10.1007/s00497-005-0012-2 · DOI
  32. Kermicle, 2010, The Zea mays sexual compatibility gene Ga2: naturally occurring alleles, their distribution, and role in reproductive isolation, J Hered., 101, 737, 10.1093/jhered/esq090 · DOI
  33. Kermicle, 2006, The Gametophyte-1 locus and reproductive isolation among Zea Mays subspecies, Maydica, 51, 219
  34. Kosakovsky Pond, 2020, Hyphy 2.5-A customizable platform for evolutionary hypothesis testing using PHYlogenies, Mol Biol Evol., 37, 295, 10.1093/molbev/msz197 · DOI
  35. Kulmuni, 2020, Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers, Philos Trans R Soc Lond B Biol Sci., 375, 20190528, 10.1098/rstb.2019.0528 · DOI
  36. Letunic, 2021, Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation, Nucleic Acids Res., 49, W293, 10.1093/nar/gkab301 · DOI
  37. Lu, 2019, A pistil-expressed pectin methylesterase confers cross-incompatibility between strains of Zea Mays, Nat Commun., 10, 2304, 10.1038/s41467-019-10259-0 · DOI
  38. Lu, 2014, Genetic and cellular analysis of cross-incompatibility in Zea Mays, Plant Reprod., 27, 19, 10.1007/s00497-013-0236-5 · DOI
  39. Mangelsdorf, 1926, The expression of Mendelian factors in the gametophyte of maize, Genetics, 11, 423, 10.1093/genetics/11.5.423 · DOI
  40. Manni, 2021, BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes, Mol Biol Evol., 38, 4647, 10.1093/molbev/msab199 · DOI · Paper page
  41. Manni, 2021, BUSCO: assessing genomic data quality and beyond, Curr Protoc., 1, e323, 10.1002/cpz1.323 · DOI
  42. Markovič, 2004, Pectin methylesterases: sequence-structural features and phylogenetic relationships, Carbohydr Res., 339, 2281, 10.1016/j.carres.2004.06.023 · DOI
  43. Matsuoka, 2002, A single domestication for maize shown by multilocus microsatellite genotyping, Proc Natl Acad Sci U S A., 99, 6080, 10.1073/pnas.052125199 · DOI
  44. McMullen, 2009, Genetic properties of the maize nested association mapping population, Science (New York, N.Y.), 325, 737, 10.1126/science.1174320 · DOI
  45. Menzel, 2010, EMT: Exact Multinomial Test: Goodness-of-Fit Test for Discrete Multivariate Data, 10.32614/cran.package.emt · DOI
  46. Moran Lauter, 2017, A pectin methylesterase ZmPme3 is expressed in gametophyte factor1-s (Ga1-s) silks and maps to that locus in maize (Zea Mays L.), Front Plant Sci., 8, 1926, 10.3389/fpls.2017.01926 · DOI
  47. Moreno, 2022, Expression atlas update: gene and protein expression in multiple Species, Nucleic Acids Res., 50, D129, 10.1093/nar/gkab1030 · DOI
  48. Murrell, 2012, Detecting individual sites subject to episodic diversifying selection, PLoS Genet., 8, e1002764, 10.1371/journal.pgen.1002764 · DOI · Paper page
  49. Nakano, 2020, Next-generation sequence databases: RNA and genomic informatics resources for plants, Plant Physiol., 182, 136, 10.1104/pp.19.00957 · DOI
  50. Nei, 2000, Molecular Evolution and Phylogenetics, 10.1093/oso/9780195135848.001.0001 · DOI · Paper page
  51. Nelson, 1952, Non-reciprocal cross-sterility in maize, Genetics, 37, 101, 10.1093/genetics/37.2.101 · DOI
  52. Piperno, 2009, Starch grain and phytolith evidence for early ninth millennium B.P. Maize from the central Balsas river valley, Mexico, Proc Natl Acad Sci U S A., 106, 5019, 10.1073/pnas.0812525106 · DOI
  53. Rushworth CA, Wardlaw AM, Ross-Ibarra J, Brandvain Y., 2022, 10.1371/journal.pbio.3001814 · DOI
  54. Schrödinger, .., The PyMOL Molecular Graphics System (Version 3.0)
  55. Schwartz, 1950, The analysis of a case of cross-sterility in maize, Proc Natl Acad Sci U S A., 36, 719, 10.1073/pnas.36.12.719 · DOI
  56. Shin, 2021, Recent advances in understanding the roles of pectin as an active participant in plant signaling networks, Plants, 10, 1712, 10.3390/plants10081712 · DOI
  57. Stamatakis, 2014, RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics (Oxford, England), 30, 1312, 10.1093/bioinformatics/btu033 · DOI · Paper page
  58. Stecher, 2020, Molecular evolutionary genetics analysis (MEGA) for macOS, Mol Biol Evol., 37, 1237, 10.1093/molbev/msz312 · DOI
  59. Stitzer, 2025, 10.1101/2025.01.22.633974 · DOI
  60. Tamura, 2021, MEGA11: molecular evolutionary genetics analysis version 11, Mol Biol Evol., 38, 3022, 10.1093/molbev/msab120 · DOI
  61. Tang, 2015, ALLMAPS: robust scaffold ordering based on multiple maps, Genome Biol., 16, 3, 10.1186/s13059-014-0573-1 · DOI
  62. Varoquaux, 2019, Transcriptomic analysis of field-droughted Sorghum from seedling to maturity reveals biotic and metabolic responses, Proc Natl Acad Sci U S A., 116, 27124, 10.1073/pnas.1907500116 · DOI
  63. Wallace, 2017, Evolutionary origins of pectin methylesterase genes associated with novel aspects of angiosperm pollen tube walls, Biochem Biophys Res Commun., 487, 509, 10.1016/j.bbrc.2017.04.027 · DOI
  64. Wang, 2018, A comparative transcriptional landscape of maize and Sorghum obtained by single-molecule sequencing, Genome Res., 28, 921, 10.1101/gr.227462.117 · DOI
  65. Wang, 2023, Mechanisms of prezygotic post-pollination reproductive barriers in plants, Front Plant Sci., 14, 1230278, 10.3389/fpls.2023.1230278 · DOI
  66. Wang, 2015, Genome alignment spanning major Poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events, Mol Plant., 8, 885, 10.1016/j.molp.2015.04.004 · DOI
  67. Wang, 2022, Three types of genes underlying the gametophyte factor1 locus cause unilateral cross incompatibility in maize, Nat Commun., 13, 4498, 10.1038/s41467-022-32180-9 · DOI
  68. Welker, 2020, Phylogenomics enables biogeographic analysis and a new subtribal classification of andropogoneae (Poaceae—panicoideae), J Syst Evol., 58, 1003, 10.1111/jse.12691 · DOI
  69. Wilkes, 1977, Hybridization of maize and teosinte, in Mexico and Guatemala and the improvement of maize, Econ Bot., 31, 254, 10.1007/BF02866877 · DOI
  70. Woodhouse, 2021, A pan-genomic approach to genome databases using maize as a model system, BMC Plant Biol., 21, 385, 10.1186/s12870-021-03173-5 · DOI
  71. Yang, 2023, Two teosintes made modern maize, Science (New York, N.Y.), 382, eadg8940, 10.1126/science.adg8940 · DOI
  72. Zeng, 2023, Natural methylation epialleles correlate with gene expression in maize, Genetics, 225, 10.1093/genetics/iyad146 · DOI
  73. Zeng, 2024, Potent pollen gene regulation by DNA glycosylases in maize, Nat Commun., 15, 8352, 10.1038/s41467-024-52620-y · DOI
  74. Zhai, 2015, Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers, Proc Natl Acad Sci U S A., 112, 3146, 10.1073/pnas.1418918112 · DOI
  75. Zhan, 2024, Premeiotic 24-nt phasiRNAs are present in the Zea genus and unique in biogenesis mechanism and molecular function, Proc Natl Acad Sci U S A., 121, e2402285121, 10.1073/pnas.2402285121 · DOI
  76. Zhang, 2023, A pollen expressed PME gene at tcb1 locus confers maize unilateral cross-incompatibility, Plant Biotechnol J., 21, 454, 10.1111/pbi.13962 · DOI
  77. Zhang, 2018, A PECTIN METHYLESTERASE gene at the maize ga1 locus confers male function in unilateral cross-incompatibility, Nat Commun., 9, 3678, 10.1038/s41467-018-06139-8 · DOI
  78. Zhou, 2022, 24-Nt phasiRNAs move from tapetal to meiotic cells in maize anthers, New Phytol., 235, 488, 10.1111/nph.18167 · DOI

Metadata

Authors
Cryan, E., Phinney, G., Seetharam, A. S., Evans, M. M. S., Kellogg, E. A., Zhan, J., Meyers, B., Kliebenstein, D. J., & Ross-Ibarra, J.
Affiliations
  • University of California, Davis (US)
  • Iowa State University (US)
  • Carnegie Institution for Science (US)
  • Huazhong Agricultural University (CN)
  • Donald Danforth Plant Science Center (US)
  • Evolution and Ecology, University of California Davis , Davis, CA 95616 ,
Corresponding author
Cryan, Elli
ORCID
Venue
GENETICS
Publisher
Oxford University Press (OUP)
Published
2025-05-08
Volume
230
Issue
3
ISSN
  • 0016-6731 (ISSN-L)
  • 1943-2631
DOI
10.1093/genetics/iyaf085
PMC
PMC12239200
OpenAlex
W4410143820
Cited by
1
References
1
Citations by year
2025: 1
FWCI
0.54
Type
journal article
Language
en
Open access
Licence
Locations
  • Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (publishedVersion, cc-by)
Funders
  • National Science Foundation (1753632)
  • Plant Genome Research and Plant-Biotic Interactions (2020754)
  • Systems and Synthetic Biology (1906486)
  • US Department of Agriculture (CA-D-PLS-2066-H 548)
  • UC Davis Plant Sciences Department
  • High-Performance Computing Core Facility
  • University of California, Davis
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
Keywords
reproductive barriers, maize, teosinte, cross-incompatibility, pectin methylesterase, gene duplication, positive selection, diversifying selection, haplotype diversity, siRNA, gene silencing, domestication, Zea
MeSH terms
Carboxylic Ester Hydrolases, Zea mays, Haplotypes, Phylogeny, Plant Proteins, Pollen, Reproduction, Selection, Genetic, Genes, Plant, Evolution, Molecular

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