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Male fertility versus sterility, cytotype, and DNA quantitative variation in seed production in diploid and tetraploid sea lavenders (Limonium sp., Plumbaginaceae) reveal diversity in reproduction modes.

ABSTRACT: The genus Limonium Miller, a complex taxonomic group, comprises annuals and perennials that can produce sexual and/or asexual seeds (apomixis). In this study, we used diverse cytogenetic and cytometric approaches to analyze male sporogenesis and gametogenesis for characterizing male reproductive output on seed production in Limonium ovalifolium and Limonium multiflorum. We showed here that the first species is mostly composed of diploid cytotypes with 2n = 16 chromosomes and the latter species by tetraploid cytotypes with 2n = 32, 34, 35, 36 chromosomes and had a genome roughly twice as big as the former one. In both species, euploid and aneuploid cytotypes with large metacentric chromosomes having decondensed interstitial sites were found within and among populations, possibly involved in chromosomal reconstructions. L. ovalifolium diploids showed regular meiosis resulting in normal tetrads, while diverse chromosome pairing and segregation irregularities leading to the formation of abnormal meiotic products are found in balanced and non-balanced L. multiflorum tetraploids. Before anther dehiscence, the characteristic unicellular, bicellular, or tricellular pollen grains showing the typical Limonium micro- or macro-reticulate exine ornamentation patterns were observed in L. ovalifolium using scanning electron microscopy. Most of these grains were viable and able to produce pollen tubes in vitro. In both balanced and unbalanced L. multiflorum tetraploids, microspores only developed until the "ring-vacuolate stage" with a collapsed morphology without the typical exine patterns, pointing to a sporophytic defect. These microspores were unviable and therefore never germinated in vitro. L. ovalifolium individuals presented larger pollen grains than those of L. multiflorum, indicating that pollen size and ploidy levels are not correlated in the Limonium system. Cytohistological studies in mature seeds from both species revealed that an embryo and a residual endosperm were present in each seed. Flow cytometric seed screens using such mature seeds showed quantitative variations in seeds ploidy level. It is concluded that male function seems to play an important role in the reproduction modes of Limonium diploids and tetraploids.

SUBMITTER: Rois AS

PROVIDER: S-EPMC3493662 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Male fertility versus sterility, cytotype, and DNA quantitative variation in seed production in diploid and tetraploid sea lavenders (Limonium sp., Plumbaginaceae) reveal diversity in reproduction modes.

Róis Ana Sofia AS Teixeira Generosa G Sharbel Timothy F TF Fuchs Jörg J Martins Sérgio S Espírito-Santo Dalila D Caperta Ana D AD

Sexual plant reproduction. 20121020 4

The genus Limonium Miller, a complex taxonomic group, comprises annuals and perennials that can produce sexual and/or asexual seeds (apomixis). In this study, we used diverse cytogenetic and cytometric approaches to analyze male sporogenesis and gametogenesis for characterizing male reproductive output on seed production in Limonium ovalifolium and Limonium multiflorum. We showed here that the first species is mostly composed of diploid cytotypes with 2n = 16 chromosomes and the latter species b ...[more]

PMID: 23086613

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Project description:Previous studies demonstrated the effects of polyploidy on various aspects of plant life. It is, however, difficult to determine which plant characteristics are responsible for fitness differences between cytotypes. We assessed the relationship between polyploidy and seed production. To separate the effects of flowering phenology, flower head size and herbivores from other possible causes, we collected data on these characteristics in single flower heads of diploid and tetraploid Centaurea phrygia in an experimental garden. We used structural equation modelling to identify the main pathways determining seed production. The results showed that the relationship between polyploidy and seed production is mediated by most of the studied factors. The different factors acted in opposing directions. Wider flower heads displayed higher above the ground suggested higher seed production in diploids. In contrast, earlier flowering and a lower abundance of herbivores suggested higher seed production in tetraploids. However, because phenology was the strongest driver of seed production in this system, the sum of all the pathways suggested greater seed production in tetraploids than in diploids. The pathway linking ploidy level directly to seed production, representing unstudied factors, was not significant. This suggests that the factors studied likely are drivers of the between-cytotype differences. Overall, this study demonstrated that tetraploids possess overall higher fitness estimated as seed production. Regardless of the patterns observed here, strong between year fluctuations in the composition and diversity of insect communities have been observed. The direction of the selection may thus vary between years. Consequently, understanding the structure of the interactions is more important for understanding the system than the overall effects of cytotype on a fitness trait in a specific year. Such knowledge can be used to model the evolution of species traits and plant-herbivore and plant-pollinator interactions in diploid-polyploid systems.

Project description:Background and aimsThe present study aims to assess the diversity and distribution of cytotypes of Aster amellus in central and eastern Europe, contributing with data to improve understanding of the evolutionary dynamics of the contact zone between diploids and hexaploids of this polyploid complex.MethodsLarge-scale cytotype screening of 4720 individuals collected in 229 populations was performed using 4',6-diamidino-2-phenylindole (DAPI) flow cytometry. Fine-scale cytotype screening was performed in the mixed-ploidy population. Reproductive variables, such as number of florets per flower head, seed set and seedling emergence, as well as ploidy level of seeds and seedlings were recorded in this population.Key resultsThe diploid-hexaploid contact zone is large and complex, reaching the Czech Republic in the west, Austria in the south, Poland in the north-east and Romania in the extreme east of the surveyed areas. Most populations presented only one cytotype, either diploid or hexaploid. In several areas of the contact zone both cytotypes were found to grow in parapatry. One mixed-ploidy population of diploids and hexaploids was detected for the first time, but no signs of hybridization were detected. In this population, diploids had a significantly lower reproductive success, and significantly higher production of intercytotype offspring, being in reproductive disadvantage in comparison with hexaploids.ConclusionsThe contact zone of diploid and hexaploid A. amellus in central and eastern Europe seems to be highly dynamic and diffuse, with both primary and secondary contacts being possible. The obtained results suggest the origin of hexaploids through diploids, overall supporting previous hypotheses that this species is autopolyploid. Data from the only mixed-ploidy population detected so far suggest that the minority cytotype exclusion is an important evolutionary mechanisms driving the prevalence of single-cytotype populations, and thus contributing to the current distributional patterns of the cytotypes of A. amellus.

Project description:Plumbaginaceae is characterized by a history of multiple taxonomic rearrangements and lacks a broad molecular phylogenetic framework. Limonium is the most species-rich genus of the family with ca. 600 species and cosmopolitan distribution. Its center of diversity is the Mediterranean region, where ca. 70% of all Limonium species are endemic. In this study, we sample 201 Limonium species covering all described infrageneric entities and spanning its wide geographic range, along with 64 species of other Plumbaginaceae genera, representing 23 out of 29 genera of the family. Additionally, 20 species of the sister family Polygonaceae were used as outgroup. Sequences of three chloroplast (trnL-F, matK, and rbcL) and one nuclear (ITS) loci were used to infer the molecular phylogeny employing maximum likelihood and Bayesian analyses. According to our results, within Plumbaginoideae, Plumbago forms a non-monophyletic assemblage, with Plumbago europaea sister to Plumbagella, while the other Plumbago species form a clade sister to Dyerophytum. Within Limonioideae, Ikonnikovia is nested in Goniolimon, rejecting its former segregation as genus distinct from Goniolimon. Limonium is divided into two major clades: Limonium subg. Pteroclados s.l., including L. sect. Pteroclados and L. anthericoides, and L. subg. Limonium. The latter is divided into three well-supported subclades: the monospecific L. sect. Limoniodendron sister to a clade comprising a mostly non-Mediterranean subclade and a Mediterranean subclade. Our results set the foundation for taxonomic proposals on sections and subsections of Limonium, namely: (a) the newly described L. sect. Tenuiramosum, created to assign L. anthericoides at the sectional rank; (b) the more restricted circumscriptions of L. sect. Limonium (= L. sect. Limonium subsect. Genuinae) and L. sect. Sarcophyllum (for the Sudano-Zambezian/Saharo-Arabian clade); (c) the more expanded circumscription of L. sect. Nephrophyllum (including species of the L. bellidifolium complex); and (d) the new combinations for L. sect. Pruinosum and L. sect. Pteroclados subsect. Odontolepideae and subsect. Nobiles.

Dataset Information

Male fertility versus sterility, cytotype, and DNA quantitative variation in seed production in diploid and tetraploid sea lavenders (Limonium sp., Plumbaginaceae) reveal diversity in reproduction modes.

Publications

Male fertility versus sterility, cytotype, and DNA quantitative variation in seed production in diploid and tetraploid sea lavenders (Limonium sp., Plumbaginaceae) reveal diversity in reproduction modes.

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