Distyly

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 (traditionally referred to as “pin”, modern nomenclature refers to them as the “long-morph” or "L-morph" flowers), or that have short styles and long stamens (traditionally referred to as “thrum”, modern nomenclature refers to these as the “short-morph” or "S-morph" flowers).[1] However, distyly can refer to any plant that has two morphs if at least one of the following characteristics between flowers produced by different plants is true; there is a difference in style length, filament length, pollen size or shape, or the surface of the stigma.[2] Most distylous plants are self-incompatible so they cannot fertilize ovules in their own flowers. Specifically these plants exhibit intra-morph self-incompatibility, flowers of the same style morph are incompatible.[3]

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

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.[4] 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.[5] The opposite is true for pollinators with smaller heads, such as bees, they uptake more pollen from short styled morphs than long styled ones.[5] The differentiation in pollinators allows the plants to reduce levels of intra-morph pollination.

Charles Darwin made the first scientific account of distyly in 1877 in his book The Different Forms of Flowers on Plants of the Same Species.[6]

Models of evolution

There are two main hypothetical models for the order in which the traits of distyly evolved, the 'selfing avoidance model' [7] and the 'pollen transfer model'. [8]

  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.[7]
  2. The pollen transfer model argues that morphological differences evolved first, and if a species is facing inbreeding depression, it may evolve SI.[8] This model can be used to explain the presence of reciprocal herkogamy in self-compatible species.[9]

Genetic control of distyly

A supergene, called the self-incompatibility (or S-) locus, is responsible for the occurrence of distyly.[9] The S-locus is composed of three tightly linked genes (S-genes) which segregate as a single unit.[9] 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.[10] The S-morph is hemizygous for the S-locus and the L-morph does not have an allelic counterpart [9]. The hemizygotic nature of the S-locus has been shown in Primula [11] , Linum [12], Fagopyrum [13], and Turnera.[14] The S-loci of Primula [15] and Turnera [14] have been completely described, meaning all S-genes have been identified.

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 [16] , Primula veris,[15] Primula oreodoxa [17], Primula vulgaris [18] and Turnera subulata.[19]

List of families with distylous species [4]

References
  1. Lewis, D. (1942). "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. Bibcode:1942RSPSB.131...13L. doi:10.1098/rspb.1942.0015. ISSN 0080-4649. JSTOR 82364. S2CID 84753102.
  2. Muenchow, Gayle (August 1982). "A loss-of-alleles model for the evolution of distyly". Heredity. 49 (1): 81–93. doi:10.1038/hdy.1982.67. ISSN 0018-067X.
  3. Barrett, Spencer C. H.; Cruzan, Mitchell B. (1994), "Incompatibility in heterostylous plants", Advances in Cellular and Molecular Biology of Plants, Springer Netherlands, pp. 189–219, doi:10.1007/978-94-017-1669-7_10, ISBN 978-90-481-4340-5
  4. Naiki, Akiyo (2012). "Heterostyly and the possibility of its breakdown by polyploidization". Plant Species Biology. 27: 3–29. doi:10.1111/j.1442-1984.2011.00363.x.
  5. Deschepper, P; Brys, R; Jacquemyn, H (2018-03-01). "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. doi:10.1093/botlinnean/box097. ISSN 0024-4074.
  6. Darwin, Charles (1877). The different forms of flowers on plants of the same species by Charles Darwin ... D. Appleton and Co. OCLC 894148387.
  7. Charlesworth, D.; Charlesworth, B. (October 1979). "A Model for the Evolution of Distyly". The American Naturalist. 114 (4): 467–498. doi:10.1086/283496. ISSN 0003-0147.
  8. Lloyd, D. G.; Webb, C. J. (1992), Barrett, Spencer C. H. (ed.), "The Selection of Heterostyly", Evolution and Function of Heterostyly, Berlin, Heidelberg: Springer Berlin Heidelberg, 15, pp. 179–207, doi:10.1007/978-3-642-86656-2_7, ISBN 978-3-642-86658-6, retrieved 2020-10-30
  9. Barrett, Spencer C. H. (November 2019). "'A most complex marriage arrangement': recent advances on heterostyly and unresolved questions". New Phytologist. 224 (3): 1051–1067. doi:10.1111/nph.16026. ISSN 0028-646X.
  10. Kappel, Christian; Huu, Cuong Nguyen; Lenhard, Michael (2017-12-16). "A short story gets longer: recent insights into the molecular basis of heterostyly". Journal of Experimental Botany. 68 (21–22): 5719–5730. doi:10.1093/jxb/erx387. ISSN 0022-0957.
  11. Li, Jinhong; Cocker, Jonathan M.; Wright, Jonathan; Webster, Margaret A.; McMullan, Mark; Dyer, Sarah; Swarbreck, David; Caccamo, Mario; Oosterhout, Cock van; Gilmartin, Philip M. (2016-12-02). "Genetic architecture and evolution of the S locus supergene in Primula vulgaris". Nature Plants. 2 (12): 1–7. doi:10.1038/nplants.2016.188. ISSN 2055-0278.
  12. Ushijima, Koichiro; Nakano, Ryohei; Bando, Mayu; Shigezane, Yukari; Ikeda, Kazuo; Namba, Yuko; Kume, Saori; Kitabata, Toshiyuki; Mori, Hitoshi; Kubo, Yasutaka (2012). "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): 317–331. doi:10.1111/j.1365-313X.2011.04792.x. ISSN 1365-313X.
  13. Yasui, Yasuo; Mori, Masashi; Aii, Jotaro; Abe, Tomoko; Matsumoto, Daiki; Sato, Shingo; Hayashi, Yoriko; Ohnishi, Ohmi; Ota, Tatsuya (2012-02-01). "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. doi:10.1371/journal.pone.0031264. ISSN 1932-6203. PMC 3270035. PMID 22312442.
  14. Shore, Joel S.; Hamam, Hasan J.; Chafe, Paul D. J.; Labonne, Jonathan D. J.; Henning, Paige M.; McCubbin, Andrew G. (2019). "The long and short of the S-locus in Turnera (Passifloraceae)". New Phytologist. 224 (3): 1316–1329. doi:10.1111/nph.15970. ISSN 1469-8137.
  15. Nowak, Michael D; Russo, Giancarlo; Schlapbach, Ralph; Huu, Cuong Nguyen; Lenhard, Michael; Conti, Elena (December 2015). "The draft genome of Primula veris yields insights into the molecular basis of heterostyly". Genome Biology. 16 (1): 12. doi:10.1186/s13059-014-0567-z. ISSN 1474-760X. PMC 4305239. PMID 25651398.
  16. Cohen, James I. (2016-12-23). "De novo Sequencing and Comparative Transcriptomics of Floral Development of the Distylous Species Lithospermum multiflorum". Frontiers in Plant Science. 7. doi:10.3389/fpls.2016.01934. ISSN 1664-462X. PMC 5179544. PMID 28066486.
  17. Zhao, Zhongtao; Luo, Zhonglai; Yuan, Shuai; Mei, Lina; Zhang, Dianxiang (December 2019). "Global transcriptome and gene co-expression network analyses on the development of distyly in Primula oreodoxa". Heredity. 123 (6): 784–794. doi:10.1038/s41437-019-0250-y. ISSN 0018-067X. PMC 6834660. PMID 31308492.
  18. Burrows, Benjamin; McCubbin, Andrew (June 2018). "Examination of S-Locus Regulated Differential Expression in Primula vulgaris Floral Development". Plants. 7 (2): 38. doi:10.3390/plants7020038. PMC 6027539. PMID 29724049.
  19. Henning, Paige M.; Shore, Joel S.; McCubbin, Andrew G. (2020-06-03). "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. doi:10.3390/plants9060713. ISSN 2223-7747. PMC 7356734. PMID 32503265.
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