Biology:Distyly

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Distyly is a type of heterostyly in which a plant demonstrates reciprocal herkogamy. This breeding system is characterized by two separate flower morphs, where individual plants produce flowers that either have long styles and short stamens (L-morph flowers), or that have short styles and long stamens (S-morph flowers).[1] However, distyly can refer to any plant that shows some degree of self-incompatibility and has two morphs if at least one of the following characteristics is true; there is a difference in style length, filament length, pollen size or shape, or the surface of the stigma.[2] Specifically these plants exhibit intra-morph self-incompatibility, flowers of the same style morph are incompatible.[3] Distylous species that do not exhibit true self-incompatibility generally show a bias towards inter-morph crosses - meaning they exhibit higher success rates when reproducing with an individual of the opposite morph.[4]

Diagram of both distylous morphs
Example of distyly in Primula. A. L-morph (pin), B. S-morph (thrum) 1. petal. 2 sepal. 3 anther. 4 pistil.

Background

The first scientific account of distyly can be found in Stephan Bejthe's Caroli book Clusii Atrebatis Rariorum aliquot stirpium [5]. Bejthe describes the two floral morphs of Primula veris. Charles Darwin popularized distyly with his account of it in his book The Different Forms of Flowers on Plants of the Same Species.[6] Darwin's book represents the first account of intramorphic self-incompatibility in distylous plants and focuses on garden experiments in which he looks at seed set of different distylous Primula. Darwin names the two floral morphs S- and L-morph, moving away from the vernacular names, Pin (for L-morph) and Thrum (for S-morph), which he states were initially assigned by florist.

Distylous species have been identified in 28 families of Angiosperm, likely evolving independently in each family.[7] This means, the system has evolved at least 28 times, though it has been suggested the system has evolved multiple times within some families.[7] Since distyly has evolved more than once, it is considered a case of convergent evolution.[7]

Reciprocal herkogamy

Reciprocal herkogamy likely evolved to prevent the pollen of the same flower from landing on its own stigma. This in turn promotes outcrossing.

In a study of Primula veris it was found that pin flowers exhibit higher rates of self-pollination and capture more pollen than the thrum morph.[8] Different pollinators show varying levels of success while pollinating the different Primula morphs, the head or proboscis length of a pollinator is positively correlated to the uptake of pollen from long styled flowers and negatively correlated for pollen uptake on short styled flowers.[9] The opposite is true for pollinators with smaller heads, such as bees, they uptake more pollen from short styled morphs than long styled ones.[9] The differentiation in pollinators allows the plants to reduce levels of intra-morph pollination.

Models of evolution

There are two main hypothetical models for the order in which the traits of distyly evolved, the 'selfing avoidance model' [10] and the 'pollen transfer model'.[11]

  1. The selfing avoidance model suggests self-incompatibility (SI) evolved first, followed by the morphological difference. It was suggested that the male component of SI would evolve first via a recessive mutation, followed by female characteristics via a dominant mutation, and finally male morphological differences would evolve via a third mutation.[10]
  2. The pollen transfer model argues that morphological differences evolved first, and if a species is facing inbreeding depression, it may evolve SI.[11] This model can be used to explain the presence of reciprocal herkogamy in self-compatible species.[7]

Genetic control of distyly

A supergene, called the self-incompatibility (or S-) locus, is responsible for the occurrence of distyly.[7] The S-locus is composed of three tightly linked genes (S-genes) which segregate as a single unit.[7]

Traditionally it was hypothesized that one S-gene controls all female aspects of distyly, one gene that controls the male morphological aspects, and one gene that determines the male mating type.[12] While this hypothesis appears to be true in Turnera,[13] it is not true in Primula [14] nor Linum.[15] The S-morph is hemizygous for the S-locus and the L-morph does not have an allelic counterpart [7]. The hemizygotic nature of the S-locus has been shown in Primula [14] , Gelsemium,[16] Linum [17][15], Fagopyrum [18][19], Turnera,[13] and Nymphoides.[20]

The presence of the S-locus results in changes to gene expression between the two floral morphs, as has been demonstrated using transcriptomic analyses of Lithospermum multiflorum [21] , Primula veris,[22] Primula oreodoxa [23], Primula vulgaris [24] and Turnera subulata.[25]

The S-locus of Fagopyrum

The S-morph of Fagopyrum contains ~2.8 Mb hemizygous region which likely represents the S-locus as it contains S-ELF4 which establishes female morphology and mating type.[18][19]

The S-locus of Gelsemium

In Gelsemium, the S-locus is composed of four genes, GeCYP, GeFRS6, and GeGA3OX are hemizygous and TAF2 appears to be allelic with a truncated copy in the L-morph.[16] GeCYP appears to share a last common ancestor (or ortholog) with the Primula S-gene CYPT. It is currently hypothesized that the for S-genes in Gelsemium were inherited as a group rather than separately.[16] This is the only known case of the S-genes being inherited as a group rather than individually.

The S-locus of Linum

In Linum the S-locus is composed of nine genes, two are LtTSS1 and LtWDR-44 the other seven are unnamed and are of unknown function.[15] LtTSS1 is hypothesized to regulate style length in the S-morph.[17] Synonymous substitution analysis of three of the S-genes suggest the S-locus in Linum evolved in a step by step manner, though only three of the nine genes were analyzed.[15]

The S-locus of Nymphoides

The S-locus of Nymphoides contains three genes NinS1, NinKHZ2, and NinBAS1.[20] NinBAS1 is only expressed in the style and is hypothetical involved in regulation of brassinosteroids, NinS1 is only expressed in the stamen, NinKHZ2 is expressed in both stamen and style.[20] Similar to other S-loci, the Nymphoides S-locus appears to have evolved via stepwise duplication events.[20]

The S-locus of Primula

In Primula the S-locus is composed of five genes, CYPT(or CYP734A50), GLOT (or GLOBOSA2), KFBT, PUMT, and CCMT. The supergene evolved in a step-by-step manner, meaning each S-gene duplicated and move to the pre-S-locus independently of the others.[26][27] Synonymous substitution analysis of the S-genes suggest the oldest S-gene in Primula is likely KFBT which likely duplicated about 104 million years ago, followed by CYPT(42.7 MYA),GLOT (37.4 MYA), CCMT(10.3 MYA).[27] It is unknown when PUMT evolved as it does not have a paralog within the Primula genome.

Of the five S-genes, two have been characterized. CYPT, a cytochrome P450 family member, is the female morphology[28] and it is the female self-incompatibility gene,[29] meaning it promotes rejection of self pollen. CYPT is likely producing these phenotypes via inactivation of brassinosteroids.[28][29] Inactivation of brassinosteroids in the S-morph by CYPT results in repression of cell elongation in the style, ultimately producing the short pistil phenotype.[28] GLOT , a MADS-BOX family member,[30] is the male morphology gene as it promotes corolla tube growth under the stamen.[26] It is unknown how the other three S-genes are contributing to distyly in Primula.

The S-locus of Turnera

In Turnera the S-locus is composed of three genes, BAHD, SPH1, and YUC6.[13] BAHD is likely an acyltransferase involved in inactivation of brassinosteroids;[31] it is both the female morphology[31] and female self-incompatibility gene.[32] YUC6 is likely involved in auxin biosynthesis based on homology; it is the male self-incompatibility gene and establishes pollen size dimorphisms.[33] SPH1 is likely involved in filament elongation based on short filament mutant analysis.[13]

Unlinked polygenic modifier in the L-morph

Little is known regarding the genetic basis of distyly in the L-morph as it has been traditionally due to the lack of an obvious loci.

In Primula, PIN5, an auxin efflux transporter, has been identified as a gene involved in promoting style length elongation in the L-morph as silencing the gene results in a short homostylous L-morph.[34] The gene is expressed in both morph, with higher levels in the L-morph compared to that of the S-morph. Silencing CYPT in the S-morph results in increased expression of PIN5, suggesting the presence of CYPT results in decreased expression of PIN5 in the S-morph.[34]

List of families with distylous species

Source:[8]


References

  1. ↑ "The Physiology of Incompatibility in Plants. I. The Effect of Temperature". Proceedings of the Royal Society of London. Series B, Biological Sciences 131 (862): 13–26. 1942. doi:10.1098/rspb.1942.0015. ISSN 0080-4649. Bibcode: 1942RSPSB.131...13L. 
  2. ↑ "A loss-of-alleles model for the evolution of distyly" (in en). Heredity 49 (1): 81–93. August 1982. doi:10.1038/hdy.1982.67. ISSN 0018-067X. 
  3. ↑ "Incompatibility in heterostylous plants". Genetic control of self-incompatibility and reproductive development in flowering plants. Advances in Cellular and Molecular Biology of Plants. 2. Springer Netherlands. 1994. pp. 189–219. doi:10.1007/978-94-017-1669-7_10. ISBN 978-90-481-4340-5. 
  4. ↑ "Intraspecific variation of self-incompatibility in the distylous plant Primula merrilliana". AoB Plants 11 (3): plz030. June 2019. doi:10.1093/aobpla/plz030. PMID 32489575. 
  5. ↑ Bejthe, Stephan (1583). Caroli Clusii Atrebatis Rariorum aliquot stirpium :per Pannoniam, Austriam, & vicinas quasdam provincias observatarum historia, quatuor libris expressa. Antverpiae: Ex officina Christophori Plantini. doi:10.5962/bhl.title.845. https://www.biodiversitylibrary.org/bibliography/845. 
  6. ↑ The different forms of flowers on plants of the same species by Charles Darwin .... D. Appleton and Co. 1877. OCLC 894148387. 
  7. ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 "'A most complex marriage arrangement': recent advances on heterostyly and unresolved questions". The New Phytologist 224 (3): 1051–1067. November 2019. doi:10.1111/nph.16026. PMID 31631362. 
  8. ↑ 8.0 8.1 "Heterostyly and the possibility of its breakdown by polyploidization" (in en). Plant Species Biology 27: 3–29. 2012. doi:10.1111/j.1442-1984.2011.00363.x. 
  9. ↑ 9.0 9.1 "The impact of flower morphology and pollinator community composition on pollen transfer in the distylous Primula veris". Botanical Journal of the Linnean Society 186 (3): 414–424. 2018-03-01. doi:10.1093/botlinnean/box097. ISSN 0024-4074. 
  10. ↑ 10.0 10.1 "A Model for the Evolution of Distyly" (in en). The American Naturalist 114 (4): 467–498. October 1979. doi:10.1086/283496. ISSN 0003-0147. 
  11. ↑ 11.0 11.1 "The Selection of Heterostyly". Evolution and Function of Heterostyly. Monographs on Theoretical and Applied Genetics. 15. Berlin, Heidelberg: Springer Berlin Heidelberg. 1992. pp. 179–207. doi:10.1007/978-3-642-86656-2_7. ISBN 978-3-642-86658-6. 
  12. ↑ "A short story gets longer: recent insights into the molecular basis of heterostyly". Journal of Experimental Botany 68 (21–22): 5719–5730. December 2017. doi:10.1093/jxb/erx387. PMID 29099983. 
  13. ↑ 13.0 13.1 13.2 13.3 "The long and short of the S-locus in Turnera (Passifloraceae)". The New Phytologist 224 (3): 1316–1329. November 2019. doi:10.1111/nph.15970. PMID 31144315. 
  14. ↑ 14.0 14.1 "Genetic architecture and evolution of the S locus supergene in Primula vulgaris". Nature Plants 2 (12): 16188. December 2016. doi:10.1038/nplants.2016.188. PMID 27909301. https://hull-repository.worktribe.com/output/3712561. 
  15. ↑ 15.0 15.1 15.2 15.3 Gutiérrez-Valencia, Juanita; Fracassetti, Marco; Berdan, Emma L.; Bunikis, Ignas; Soler, Lucile; Dainat, Jacques; Kutschera, Verena E.; Losvik, Aleksandra et al. (2022). "Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level" (in en). Current Biology 32 (20): 4360–4371.e6. doi:10.1016/j.cub.2022.08.042. PMID 36087578. 
  16. ↑ 16.0 16.1 16.2 Zhao, Zhongtao; Zhang, Yu; Shi, Miaomiao; Liu, Zhaoying; Xu, Yuanqing; Luo, Zhonglai; Yuan, Shuai; Tu, Tieyao et al. (2022-11-22). "Genomic evidence supports the genetic convergence of a supergene controlling the distylous floral syndrome" (in en). New Phytologist 237 (2): 601–614. doi:10.1111/nph.18540. ISSN 0028-646X. PMID 36239093. https://onlinelibrary.wiley.com/doi/10.1111/nph.18540. 
  17. ↑ 17.0 17.1 "Isolation of the floral morph-related genes in heterostylous flax (Linum grandiflorum): the genetic polymorphism and the transcriptional and post-transcriptional regulations of the S locus". The Plant Journal 69 (2): 317–31. January 2012. doi:10.1111/j.1365-313X.2011.04792.x. PMID 21923744. 
  18. ↑ 18.0 18.1 "S-LOCUS EARLY FLOWERING 3 is exclusively present in the genomes of short-styled buckwheat plants that exhibit heteromorphic self-incompatibility". PLOS ONE 7 (2): e31264. 2012-02-01. doi:10.1371/journal.pone.0031264. PMID 22312442. Bibcode: 2012PLoSO...731264Y. 
  19. ↑ 19.0 19.1 Fawcett, Jeffrey A.; Takeshima, Ryoma; Kikuchi, Shinji; Yazaki, Euki; Katsube-Tanaka, Tomoyuki; Dong, Yumei; Li, Meifang; Hunt, Harriet V. et al. (2023). "Genome sequencing reveals the genetic architecture of heterostyly and domestication history of common buckwheat" (in en). Nature Plants 9 (8): 1236–1251. doi:10.1038/s41477-023-01474-1. ISSN 2055-0278. https://www.nature.com/articles/s41477-023-01474-1. 
  20. ↑ 20.0 20.1 20.2 20.3 Yang, Jingshan; Xue, Haoran; Li, Zhizhong; Zhang, Yue; Shi, Tao; He, Xiangyan; Barrett, Spencer C. H.; Wang, Qingfeng et al. (2023-09-17). "Haplotype‐resolved genome assembly provides insights into the evolution of S ‐locus supergene in distylous Nymphoides indica" (in en). New Phytologist 240 (5): 2058–2071. doi:10.1111/nph.19264. ISSN 0028-646X. 
  21. ↑ "De novo Sequencing and Comparative Transcriptomics of Floral Development of the Distylous Species Lithospermum multiflorum". Frontiers in Plant Science 7: 1934. 2016-12-23. doi:10.3389/fpls.2016.01934. PMID 28066486. 
  22. ↑ "The draft genome of Primula veris yields insights into the molecular basis of heterostyly". Genome Biology 16 (1): 12. January 2015. doi:10.1186/s13059-014-0567-z. PMID 25651398. 
  23. ↑ "Global transcriptome and gene co-expression network analyses on the development of distyly in Primula oreodoxa". Heredity 123 (6): 784–794. December 2019. doi:10.1038/s41437-019-0250-y. PMID 31308492. 
  24. ↑ "Examination of S-Locus Regulated Differential Expression in Primula vulgaris Floral Development". Plants 7 (2): 38. May 2018. doi:10.3390/plants7020038. PMID 29724049. 
  25. ↑ "Transcriptome and Network Analyses of Heterostyly in Turnera subulata Provide Mechanistic Insights: Are S-Loci a Red-Light for Pistil Elongation?". Plants 9 (6): 713. June 2020. doi:10.3390/plants9060713. PMID 32503265. 
  26. ↑ 26.0 26.1 Huu, Cuong Nguyen; Keller, Barbara; Conti, Elena; Kappel, Christian; Lenhard, Michael (2020-09-15). "Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene" (in en). Proceedings of the National Academy of Sciences 117 (37): 23148–23157. doi:10.1073/pnas.2006296117. ISSN 0027-8424. PMID 32868445. 
  27. ↑ 27.0 27.1 Potente, Giacomo; Léveillé-Bourret, Étienne; Yousefi, Narjes; Choudhury, Rimjhim Roy; Keller, Barbara; Diop, Seydina Issa; Duijsings, Daniël; Pirovano, Walter et al. (2022-02-03). de Meaux, Juliette. ed. "Comparative Genomics Elucidates the Origin of a Supergene Controlling Floral Heteromorphism" (in en). Molecular Biology and Evolution 39 (2): msac035. doi:10.1093/molbev/msac035. ISSN 0737-4038. PMID 35143659. PMC 8859637. https://academic.oup.com/mbe/article/doi/10.1093/molbev/msac035/6526404. 
  28. ↑ 28.0 28.1 28.2 Huu, Cuong Nguyen; Kappel, Christian; Keller, Barbara; Sicard, Adrien; Takebayashi, Yumiko; Breuninger, Holger; Nowak, Michael D; Bäurle, Isabel et al. (2016-09-06). Hardtke, Christian S. ed. "Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses". eLife 5: e17956. doi:10.7554/eLife.17956. ISSN 2050-084X. PMID 27596932. 
  29. ↑ 29.0 29.1 Huu, Cuong Nguyen; Plaschil, Sylvia; Himmelbach, Axel; Kappel, Christian; Lenhard, Michael (2022). "Female self-incompatibility type in heterostylous Primula is determined by the brassinosteroid-inactivating cytochrome P450 CYP734A50" (in en). Current Biology 32 (3): 671–676.e5. doi:10.1016/j.cub.2021.11.046. PMID 34906354. 
  30. ↑ Burrows, Benjamin A.; McCubbin, Andrew G. (2017). "Sequencing the genomic regions flanking S-linked PvGLO sequences confirms the presence of two GLO loci, one of which lies adjacent to the style-length determinant gene CYP734A50" (in en). Plant Reproduction 30 (1): 53–67. doi:10.1007/s00497-017-0299-9. ISSN 2194-7953. PMID 28229234. http://link.springer.com/10.1007/s00497-017-0299-9. 
  31. ↑ 31.0 31.1 Matzke, Courtney M.; Shore, Joel S.; Neff, Michael M.; McCubbin, Andrew G. (2020-11-13). "The Turnera Style S-Locus Gene TsBAHD Possesses Brassinosteroid-Inactivating Activity When Expressed in Arabidopsis thaliana" (in en). Plants 9 (11): 1566. doi:10.3390/plants9111566. ISSN 2223-7747. PMID 33202834. 
  32. ↑ Matzke, Courtney M.; Hamam, Hasan J.; Henning, Paige M.; Dougherty, Kyra; Shore, Joel S.; Neff, Michael M.; McCubbin, Andrew G. (2021-09-30). "Pistil Mating Type and Morphology Are Mediated by the Brassinosteroid Inactivating Activity of the S-Locus Gene BAHD in Heterostylous Turnera Species" (in en). International Journal of Molecular Sciences 22 (19): 10603. doi:10.3390/ijms221910603. ISSN 1422-0067. PMID 34638969. 
  33. ↑ Henning, Paige M.; Shore, Joel S.; McCubbin, Andrew G. (2022-10-08). "The S-Gene YUC6 Pleiotropically Determines Male Mating Type and Pollen Size in Heterostylous Turnera (Passifloraceae): A Novel Neofunctionalization of the YUCCA Gene Family" (in en). Plants 11 (19): 2640. doi:10.3390/plants11192640. ISSN 2223-7747. PMID 36235506. 
  34. ↑ 34.0 34.1 Liu, Ying; Si, Weijia; Fu, Sitong; Wang, Jia; Cheng, Tangren; Zhang, Qixiang; Pan, Huitang (2024-01-08). "PfPIN5 promotes style elongation by regulating cell length in Primula forbesii French". Annals of Botany. doi:10.1093/aob/mcae004. ISSN 0305-7364. https://doi.org/10.1093/aob/mcae004. 



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