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]

Contents

Diagram of both distylous morphs Distyly.png
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. Distyly primula.jpg
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 by repressing expression of PIN5, ultimately producing the short pistil phenotype. [28] [30] GLOT , a MADS-BOX family member, [31] 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; [32] it is both the female morphology [32] and female self-incompatibility gene. [33] YUC6 is likely involved in auxin biosynthesis based on homology; it is the male self-incompatibility gene and establishes pollen size dimorphisms. [34] SPH1 is likely involved in filament elongation based on short filament mutant analysis. [13]

List of families with distylous species

Source: [8]

Related Research Articles

<span class="mw-page-title-main">Coevolution</span> Two or more species influencing each others evolution

In biology, coevolution occurs when two or more species reciprocally affect each other's evolution through the process of natural selection. The term sometimes is used for two traits in the same species affecting each other's evolution, as well as gene-culture coevolution.

<span class="mw-page-title-main">Polymorphism (biology)</span> Occurrence of two or more clearly different morphs or forms in the population of a species

In biology, polymorphism is the occurrence of two or more clearly different morphs or forms, also referred to as alternative phenotypes, in the population of a species. To be classified as such, morphs must occupy the same habitat at the same time and belong to a panmictic population.

<span class="mw-page-title-main">Plant reproductive morphology</span> Parts of plant enabling sexual reproduction

Plant reproductive morphology is the study of the physical form and structure of those parts of plants directly or indirectly concerned with sexual reproduction.

Self-incompatibility (SI) is a general name for several genetic mechanisms that prevent self-fertilization in sexually reproducing organisms, and thus encourage outcrossing and allogamy. It is contrasted with separation of sexes among individuals (dioecy), and their various modes of spatial (herkogamy) and temporal (dichogamy) separation.

<span class="mw-page-title-main">Heterostyly</span> Two different types of flowers (style) on same plant

Heterostyly is a unique form of polymorphism and herkogamy in flowers. In a heterostylous species, two or three morphological types of flowers, termed "morphs", exist in the population. On each individual plant, all flowers share the same morph. The flower morphs differ in the lengths of the pistil and stamens, and these traits are not continuous. The morph phenotype is genetically linked to genes responsible for a unique system of self-incompatibility, termed heteromorphic self-incompatibility, that is, the pollen from a flower on one morph cannot fertilize another flower of the same morph.

A supergene is a chromosomal region encompassing multiple neighboring genes that are inherited together because of close genetic linkage, i.e. much less recombination than would normally be expected. This mode of inheritance can be due to genomic rearrangements between supergene variants.

<span class="mw-page-title-main">Flower</span> Reproductive structure in flowering plants

A flower, also known as a bloom or blossom, is the reproductive structure found in flowering plants. Flowers consist of a combination of vegetative organs – sepals that enclose and protect the developing flower, petals that attract pollinators, and reproductive organs that produce gametophytes, which in flowering plants produce gametes. The male gametophytes, which produce sperm, are enclosed within pollen grains produced in the anthers. The female gametophytes are contained within the ovules produced in the carpels.

<span class="mw-page-title-main">Ornithophily</span> Pollination by birds

Ornithophily or bird pollination is the pollination of flowering plants by birds. This sometimes coevolutionary association is derived from insect pollination (entomophily) and is particularly well developed in some parts of the world, especially in the tropics, Southern Africa, and on some island chains. The association involves several distinctive plant adaptations forming a "pollination syndrome". The plants typically have colourful, often red, flowers with long tubular structures holding ample nectar and orientations of the stamen and stigma that ensure contact with the pollinator. Birds involved in ornithophily tend to be specialist nectarivores with brushy tongues and long bills, that are either capable of hovering flight or light enough to perch on the flower structures.

<span class="mw-page-title-main">Palynivore</span> Group of herbivorous animals

In zoology, a palynivore /pəˈlɪnəvɔːɹ/, meaning "pollen eater" is an herbivorous animal which selectively eats the nutrient-rich pollen produced by angiosperms and gymnosperms. Most true palynivores are insects or mites. The category in its strictest application includes most bees, and a few kinds of wasps, as pollen is often the only solid food consumed by all life stages in these insects. However, the category can be extended to include more diverse species. For example, palynivorous mites and thrips typically feed on the liquid content of the pollen grains without actually consuming the exine, or the solid portion of the grain. Additionally, the list is expanded greatly if one takes into consideration species where either the larval or adult stage feeds on pollen, but not both. There are other wasps which are in this category, as well as many beetles, flies, butterflies, and moths. One such example of a bee species that only consumes pollen in its larval stage is the Apis mellifera carnica. There is a vast array of insects that will feed opportunistically on pollen, as will various birds, orb-weaving spiders and other nectarivores.

<span class="mw-page-title-main">Pollination syndrome</span> Flower traits that attract pollinators

Pollination syndromes are suites of flower traits that have evolved in response to natural selection imposed by different pollen vectors, which can be abiotic or biotic, such as birds, bees, flies, and so forth through a process called pollinator-mediated selection. These traits include flower shape, size, colour, odour, reward type and amount, nectar composition, timing of flowering, etc. For example, tubular red flowers with copious nectar often attract birds; foul smelling flowers attract carrion flies or beetles, etc.

Tristyly is a rare floral polymorphism that consists of three floral morphs that differ in regard to the length of the stamens and style within the flower. This type of floral mechanism is thought to encourage outcross pollen transfer and is usually associated with heteromorphic self-incompatibility to reduce inbreeding. It is an example of heterostyly and reciprocal herkogamy, like distyly, which is the more common form of heterostyly. Darwin first described tristylous species in 1877 in terms of the incompatibility of these three morphs.

<i>Turnera</i> Genus of flowering plants

Turnera is a genus of flowering plants in the passionflower family, Passifloraceae. It contains more than 100 species native to tropical and subtropical America. The name honours English naturalist William Turner (1508–1568). It was previously placed in the family Turneraceae.

<span class="mw-page-title-main">Gynodioecy</span> Coexistence of female and hermaphrodite within a population

Gynodioecy is a rare breeding system that is found in certain flowering plant species in which female and hermaphroditic plants coexist within a population. Gynodioecy is the evolutionary intermediate between hermaphroditism and dioecy.

<i>Arcytophyllum</i> Genus of flowering plants

Arcytophyllum is a genus of flowering plants in the family Rubiaceae. The genus contains 18 species, distributed from New Mexico to Bolivia.

<i>Turnera subulata</i> Species of flowering plant

Turnera subulata is a species of flowering plant in the passionflower family known by the common names white buttercup, sulphur alder, politician's flower, dark-eyed turnera, and white alder. Despite its names, it is not related to the buttercups or the alders. It is native to Central and South America, from Panama south to Brazil. It is well known in many other places as an introduced species, such as Malaysia, Indonesia, several other Pacific Islands, the Caribbean, and Florida in the United States.

<i>Hypericum aegypticum</i> Species of flowering plant in the St Johns wort family Hypericaceae

Hypericum aegypticum is a species of flowering plant of the St. John's wort family (Hypericaceae) which is native to the Eastern Mediterranean. It was described by Carl Linnaeus in the second volume of his Species Plantarum in 1753, who named it after Egypt despite it not being distributed there. The plant is commonly known as shrubby St. John's wort or Egyptian St. John's wort in English. Like other members of section Adenotrias, it is found among limestone rocks in coastal areas. While it has been evaluated as threatened on the island of Malta, the species has no legal protections.

<span class="mw-page-title-main">Monocotyledon reproduction</span> Flowering plant reproduction system

The monocots are one of the two major groups of flowering plants, the other being the dicots. In order to reproduce they utilize various strategies such as employing forms of asexual reproduction, restricting which individuals they are sexually compatible with, or influencing how they are pollinated. Nearly all reproductive strategies that evolved in the dicots have independently evolved in monocots as well. Despite these similarities and their close relatedness, monocots and dicots have distinct traits in their reproductive biologies.

June Nasrallah is Barbara McClintock Professor in the Plant Biology Section of the School of Integrative Plant Science at Cornell University. Her research focuses on plant reproductive biology and the cell-cell interactions that underlie self-incompatibility in plants belonging to the mustard (Brassicaceae) family. She was elected to the US National Academy of Sciences in 2003 for this work and her contributions generally to our understanding of receptor-based signaling in plants.

<span class="mw-page-title-main">Pollinator-mediated selection</span> Process in which pollenators effects a plants evolution

Pollinator-mediated selection is an evolutionary process occurring in flowering plants, in which the foraging behavior of pollinators differentially selects for certain floral traits. Flowering plant are a diverse group of plants that produce seeds. Their seeds differ from those of gymnosperms in that they are enclosed within a fruit. These plants display a wide range of diversity when it comes to the phenotypic characteristics of their flowers, which attracts a variety of pollinators that participate in biotic interactions with the plant. Since many plants rely on pollen vectors, their interactions with them influence floral traits and also favor efficiency since many vectors are searching for floral rewards like pollen and nectar. Examples of pollinator-mediated selected traits could be those involving the size, shape, color and odor of flowers, corolla tube length and width, size of inflorescence, floral rewards and amount, nectar guides, and phenology. Since these types of traits are likely to be involved in attracting pollinators, they may very well be the result of selection by the pollinators themselves.

<span class="mw-page-title-main">Monoecy</span> Sexual system in seed plants

Monoecy is a sexual system in seed plants where separate male and female cones or flowers are present on the same plant. It is a monomorphic sexual system comparable with gynomonoecy, andromonoecy and trimonoecy, and contrasted with dioecy where individual plants produce cones or flowers of only one sex and with bisexual or hermaphroditic plants in which male and female gametes are produced in the same flower.

References

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  31. ↑ 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". Plant Reproduction. 30 (1): 53–67. doi:10.1007/s00497-017-0299-9. ISSN   2194-7953. PMID   28229234. S2CID   22910136.
  32. 1 2 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". Plants. 9 (11): 1566. doi: 10.3390/plants9111566 . ISSN   2223-7747. PMC   7697239 . PMID   33202834.
  33. ↑ 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". International Journal of Molecular Sciences. 22 (19): 10603. doi: 10.3390/ijms221910603 . ISSN   1422-0067. PMC   8509066 . PMID   34638969.
  34. ↑ 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". Plants. 11 (19): 2640. doi: 10.3390/plants11192640 . ISSN   2223-7747. PMC   9572539 . PMID   36235506.
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