CoChat
Sign Up
Cited by 25Evolution and Genetic DynamicsAnimal Behavior and ReproductionPlant Diversity and Evolution

Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower

Open access
Wilkinson, Melanie J., Roda, Federico, Walter, Greg M., James, Maddie E., Nipper, Rick, Walsh, Jessica, Allen, Scott L., North, Henry L. +2 more·2021·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.2004901118PMC PMC8617494

Published version of a preprint

Open this paper in CoChat — free account

Abstract

We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. Our experiments revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. Using the advanced hybrid population, we discovered that individuals with extreme differences in gravitropism had more sterile crosses than individuals with similar gravitropic responses, which were largely fertile, indicating that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus revealing an evolutionary connection between local adaptation and the origin of new species.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.2004901118

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Wilkinson et al. (2021) identified candidate genes for gravitropism and associated hybrid sterility by genotyping the tails of the gravitropic distribution in F11 hybrid populations between Senecio ecotypes.

    “Likewise, Wilkinson et al. (2021) identified candidate genes for gravitropism (and associated hybrid sterility) by genotyping the tails of the gravitropic distribution in F11 hybrid populations between ecotypes of Senecio.”

    From Genomics of plant speciation (2023) · cites this paper as Wilkinson et al. (2021)

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 77 · Cited by 25

Research works printed but not linked: 62

  1. [3]H. D. Rundle, M. C. Whitlock, A genetic interpretation of ecologically dependent isolation. Evolution 55, 198– 201 (2001). 11263739
  2. [4]O. Seehausen, Genomics and the origin of species. Nat. Rev. Genet. 15, 176– 192 (2014). 24535286
  3. [5]E. Baack, M. C. Melo, L. H. Rieseberg, D. Ortiz-Barrientos, The origins of reproductive isolation in plants. New Phytol. 207, 968– 984 (2015). 25944305
  4. [6]J. M. Coughlan, D. R. Matute, The importance of intrinsic postzygotic barriers throughout the speciation process. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190533 (2020). 32654642 PMC7423280
  5. [7]D. Schluter, G. L. Conte, Genetics and ecological speciation. Proc. Natl. Acad. Sci. U.S.A. 106, 9955– 9962 (2009). 19528639 PMC2702799
  6. [8]D. B. Lowry, R. C. Rockwood, J. H. Willis, Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62, 2196– 2214 (2008). 18637837 PMC11110535
  7. [9]K. Bomblies, D. Weigel, Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8, 382– 393 (2007). 17404584
  8. [11]M. Kirkpatrick, N. Barton, Chromosome inversions, local adaptation and speciation. Genetics 173, 419– 434 (2006). 16204214 PMC1461441
  9. [12]A. F. Agrawal, J. L. Feder, P. Nosil, Ecological divergence and the origins of intrinsic postmating isolation with gene flow. Int. J. Ecol. 2011, 435357 (2011).
  10. [13]A. Burt, R. Trivers, Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard University Press, 2006).
  11. [14]S. A. Johnston, T. P. M. den Nijs, S. J. Peloquin, R. E. Hanneman Jr., The significance of genic balance to endosperm development in interspecific crosses. Theor. Appl. Genet. 57, 5– 9 (1980). 24302359
  12. [15]D. C. Presgraves, The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11, 175– 180 (2010). 20051985
  13. [19]F. Roda, Convergence and divergence during the adaptation to similar environments by an Australian groundsel. Evolution 67, 2515– 2529 (2013). 24033164
  14. [20]M. E. James, Phenotypic and genotypic parallel evolution in parapatric ecotypes of Senecio. Evolution. 10.1111/evo.14387 (2021). PMC9299460 34687472 · DOI
  15. [21]M. Xu, L. Zhu, H. Shou, P. Wu, A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674– 1681 (2005). 16085936
  16. [23]A. Gallavotti, The role of auxin in shaping shoot architecture. J. Exp. Bot. 64, 2593– 2608 (2013). 23709672
  17. [24]M. A. Domagalska, O. Leyser, Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12, 211– 221 (2011). 21427763
  18. [25]E. Sundberg, L. Østergaard, Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb. Perspect. Biol. 1, a001628 (2009). 20457563 PMC2882118
  19. [26]F. Roda, G. M. Walter, R. Nipper, D. Ortiz-Barrientos, Genomic clustering of adaptive loci during parallel evolution of an Australian wildflower. Mol. Ecol. 26, 3687– 3699 (2017). 28429828
  20. [27]J. Friml, Auxin transport - Shaping the plant. Curr. Opin. Plant Biol. 6, 7– 12 (2003). 12495745
  21. [28]D. Lopez, K. Tocquard, J.-S. Venisse, V. Legué, P. Roeckel-Drevet, Gravity sensing, a largely misunderstood trigger of plant orientated growth. Front Plant Sci 5, 610 (2014). 25414717 PMC4220637
  22. [29]D. Sang, Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 111, 11199– 11204 (2014). 25028496 PMC4121785
  23. [30]G. M. Walter, Diversification across a heterogeneous landscape. Evolution 70, 1979– 1992 (2016). 27436057
  24. [31]F. Roda, Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex. Mol. Ecol. 22, 2941– 2952 (2013). 23710896
  25. [33]M. C. Melo, A. Grealy, B. Brittain, G. M. Walter, D. Ortiz-Barrientos, Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel. New Phytol. 203, 323– 334 (2014). 24684207
  26. [34]G. M. Walter, Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation. Evol. Lett. 4, 302– 316 (2020). 32774880 PMC7403682
  27. [35]M. Yamamoto, K. T. Yamamoto, Differential effects of 1-naphthaleneacetic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid on the gravitropic response of roots in an auxin-resistant mutant of arabidopsis, aux1. Plant Cell Physiol. 39, 660– 664 (1998). 9697346
  28. [36]I. Ottenschläger, Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. U.S.A. 100, 2987– 2991 (2003). 12594336 PMC151453
  29. [37]E. B. Blancaflor, Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am. J. Bot. 100, 143– 152 (2013). 23002165
  30. [38]D. B. Lowry, D. Popovic, D. J. Brennan, L. M. Holeski, Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus. Evolution 73, 1168– 1181 (2019). 30793293
  31. [39]L. Barboza, Arabidopsis semidwarfs evolved from independent mutations in GA20ox1, ortholog to green revolution dwarf alleles in rice and barley. Proc. Natl. Acad. Sci. U.S.A. 110, 15818– 15823 (2013). 24023067 PMC3785751
  32. [40]G. M. Walter, Senecio as a model system for integrating studies of genotype, phenotype and fitness. New Phytol. 226, 326– 344 (2020). 31951018
  33. [42]P. Ranocha, Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat. Commun. 4, 2625 (2013). 24129639 PMC3826630
  34. [43]P. Ranocha, Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J. 63, 469– 483 (2010). 20497379
  35. [44]X. Dai, K. Hayashi, H. Nozaki, Y. Cheng, Y. Zhao, Genetic and chemical analyses of the action mechanisms of sirtinol in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 102, 3129– 3134 (2005). 15710899 PMC549487
  36. [45]M. Sagi, C. Scazzocchio, R. Fluhr, The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J. 31, 305– 317 (2002). 12164810
  37. [46]S. Promchuea, Y. Zhu, Z. Chen, J. Zhang, Z. Gong, ARF2 coordinates with PLETHORAs and PINs to orchestrate ABA-mediated root meristem activity in Arabidopsis. J. Integr. Plant Biol. 59, 30– 43 (2017). 28074634
  38. [48]A. L. Sweigart, L. E. Flagel, Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in Mimulus. Genetics 199, 543– 554 (2015). 25428983 PMC4317661
  39. [49]W. Beeftink, J. Rozema, A. Huiskes, Ecology of Coastal Vegetation (Springer, 1985), vol. 6.
  40. [52]G. M. Crutsinger, S. Y. Strauss, J. A. Rudgers, Genetic variation within a dominant shrub species determines plant species colonization in a coastal dune ecosystem. Ecology 91, 1237– 1243 (2010). 20462137
  41. [53]T. Li, Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche. Nat. Commun. 10, 726 (2019). 30760714 PMC6374474
  42. [54]V. Naser, E. Shani, Auxin response under osmotic stress. Plant Mol. Biol. 91, 661– 672 (2016). 27052306
  43. [55]T. van den Berg, R. A. Korver, C. Testerink, K. H. Ten Tusscher, Modeling halotropism: A key role for root tip architecture and reflux loop remodeling in redistributing auxin. Development 143, 3350– 3362 (2016). 27510970 PMC5047658
  44. [56]C. S. Galvan-Ampudia, Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23, 2044– 2050 (2013). 24094855
  45. [57]B. A. Gould, Y. Chen, D. B. Lowry, Pooled ecotype sequencing reveals candidate genetic mechanisms for adaptive differentiation and reproductive isolation. Mol. Ecol. 26, 163– 177 (2017). 27747958
  46. [58]D. B. Lowry, J. H. Willis, A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8, e1000500 (2010). 20927411 PMC2946948
  47. [59]D. B. Lowry, M. C. Hall, D. E. Salt, J. H. Willis, Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. 183, 776– 788 (2009). 19549130
  48. [60]A. VanWallendael, A molecular view of plant local adaptation: Incorporating stress-response networks. Annu. Rev. Plant Biol. 70, 559– 583 (2019). 30786237
  49. [61]M. Turelli, L. C. Moyle, Asymmetric postmating isolation: Darwin’s corollary to Haldane’s rule. Genetics 176, 1059– 1088 (2007). 17435235 PMC1894575
  50. [62]H.-H. Wang, Close arrangement of CARK3 and PMEIL affects ABA-mediated pollen sterility in Arabidopsis thaliana. Plant Cell Environ. 43, 2699– 2711 (2020). 32816352
  51. [63]Y. Hou, Maternal ENODLs are required for pollen tube reception in Arabidopsis. Curr. Biol. 26, 2343– 2350 (2016). 27524487 PMC5522746
  52. [64]Y. Yang, U. Z. Hammes, C. G. Taylor, D. P. Schachtman, E. Nielsen, High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123– 1127 (2006). 16677815
  53. [65]C. A. Schneider, W. S. Rasband, K. W. Eliceiri, NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671– 675 (2012). 22930834 PMC5554542
  54. [66]G. Rigó, Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25, 1592– 1608 (2013). 23673979 PMC3694694
  55. [67]A. M. Rashotte, S. R. Brady, R. C. Reed, S. J. Ante, G. K. Muday, Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 122, 481– 490 (2000). 10677441 PMC58885
  56. [69]R. G. Shaw, C. J. Geyer, S. Wagenius, H. H. Hangelbroek, J. R. Etterson, Unifying life-history analyses for inference of fitness and population growth. Am. Nat. 172, E35– E47 (2008). 18500940
  57. [71]J. D. Clarke, Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb. Protoc. 2009, pdb.prot5177 (2009). 20147112
  58. [72]H. Liu, “Developing genomic resources for an emerging ecological model species Senecio lautus,” PhD thesis, School of Biological Sciences, The University of Queensland (2015), 274 pp.
  59. [73]N. A. Baird, Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3, e3376 (2008). 18852878 PMC2557064
  60. [74]B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009). 19261174 PMC2690996
  61. [75]H. Li, The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078– 2079 (2009). 19505943 PMC2723002
  62. [76]S. F. Altschul, W. Gish, W. Miller, E. W. Myers, D. J. Lipman, Basic local alignment search tool. J. Mol. Biol. 215, 403– 410 (1990). 2231712

Authors
Wilkinson, M. J., Roda, F., Walter, G. M., James, M. E., Nipper, R., Walsh, J., Allen, S. L., North, H. L., Beveridge, C. A., & Ortiz-Barrientos, D.
Affiliations
  • The University of Queensland (AU)
  • Floragenex, Inc., Portland, OR 97239;
  • School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Corresponding author
Wilkinson, Melanie J.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2021-11-17
Volume
118
Issue
47
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.2004901118
PMC
PMC8617494
OpenAlex
W3211482424
Cited by
25
References
77
Citations by year
2026: 3 · 2025: 5 · 2024: 2 · 2023: 7 · 2022: 5 · 2021: 3
FWCI
2.40
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
Australian Research Council (DP190103039, DP0986172, DP0986175, DP140103774, DP120104559)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
Keywords
shoot gravitropism, hybrid sterility, local adaptation, plant height, recombination, natural selection, speciation, genetic correlation
MeSH terms
Adaptation, Physiological, Australia, Indoleacetic Acids, Infertility, Phenotype, Selection, Genetic, Senecio, Sulfurtransferases, Genetic Variation, Plant Shoots, Gravitropism, Arabidopsis Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review