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      A First Glimpse of Wild Lupin Karyotype Variation As Revealed by Comparative Cytogenetic Mapping

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          Abstract

          Insight into plant genomes at the cytomolecular level provides useful information about their karyotype structure, enabling inferences about taxonomic relationships and evolutionary origins. The Old World lupins (OWL) demonstrate a high level of genomic diversification involving variation in chromosome numbers (2 n = 32–52), basic chromosome numbers ( x = 5–7, 9, 13) and in nuclear genome size (2C DNA = 0.97–2.68 pg). Lupins comprise both crop and wild species and provide an intriguing system to study karyotype evolution. In order to investigate lupin chromosome structure, heterologous FISH was used. Sixteen BACs that had been generated as chromosome markers for the reference species, Lupinus angustifolius, were used to identify chromosomes in the wild species and explore karyotype variation. While all “single-locus” in L. angustifolius, in the wild lupins these clones proved to be “single-locus,” “single-locus” with additional signals, “repetitive” or had no detectable BAC-FISH signal. The diverse distribution of the clones in the targeted genomes suggests a complex evolution history, which possibly involved multiple chromosomal changes such as fusions/fissions and repetitive sequence amplification. Twelve BACs were sequenced and we found numerous transposable elements including DNA transposons as well as LTR and non-LTR retrotransposons with varying quantity and composition among the different lupin species. However, at this preliminary stage, no correlation was observed between the pattern of BAC-FISH signals and the repeat content in particular BACs. Here, we describe the first BAC-based chromosome-specific markers for the wild species: L. cosentinii, L. cryptanthus, L. pilosus, L. micranthus and one New World lupin, L. multiflorus. These BACs could constitute the basis for an assignment of the chromosomal and genetic maps of other lupins, e.g., L. albus and L. luteus. Moreover, we identified karyotype variation that helps illustrate the relationships between the lupins and the extensive cytological diversity within this group. In this study we premise that lupin genomes underwent at least two rounds of fusion and fission events resulting in the reduction in chromosome number from 2 n = 52 through 2 n = 40 to 2 n = 32, followed by chromosome number increment to 2 n = 42.

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          Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium.

          The DNA content of eukaryotic nuclei (C-value) varies approximately 200,000-fold, but there is only a approximately 20-fold variation in the number of protein-coding genes. Hence, most C-value variation is ascribed to the repetitive fraction, although little is known about the evolutionary dynamics of the specific components that lead to genome size variation. To understand the modes and mechanisms that underlie variation in genome composition, we generated sequence data from whole genome shotgun (WGS) libraries for three representative diploid (n = 13) members of Gossypium that vary in genome size from 880 to 2460 Mb (1C) and from a phylogenetic outgroup, Gossypioides kirkii, with an estimated genome size of 588 Mb. Copy number estimates including all dispersed repetitive sequences indicate that 40%-65% of each genome is composed of transposable elements. Inspection of individual sequence types revealed differential, lineage-specific expansion of various families of transposable elements among the different plant lineages. Copia-like retrotransposable element sequences have differentially accumulated in the Gossypium species with the smallest genome, G. raimondii, while gypsy-like sequences have proliferated in the lineages with larger genomes. Phylogenetic analyses demonstrated a pattern of lineage-specific amplification of particular subfamilies of retrotransposons within each species studied. One particular group of gypsy-like retrotransposon sequences, Gorge3 (Gossypium retrotransposable gypsy-like element), appears to have undergone a massive proliferation in two plant lineages, accounting for a major fraction of genome-size change. Like maize, Gossypium has undergone a threefold increase in genome size due to the accumulation of LTR retrotransposons over the 5-10 Myr since its origin.
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            Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling.

            Replicate radiations provide powerful comparative systems to address questions about the interplay between opportunity and innovation in driving episodes of diversification and the factors limiting their subsequent progression. However, such systems have been rarely documented at intercontinental scales. Here, we evaluate the hypothesis of multiple radiations in the genus Lupinus (Leguminosae), which exhibits some of the highest known rates of net diversification in plants. Given that incomplete taxon sampling, background extinction, and lineage-specific variation in diversification rates can confound macroevolutionary inferences regarding the timing and mechanisms of cladogenesis, we used Bayesian relaxed clock phylogenetic analyses as well as MEDUSA and BiSSE birth-death likelihood models of diversification, to evaluate the evolutionary patterns of lineage accumulation in Lupinus. We identified 3 significant shifts to increased rates of net diversification (r) relative to background levels in the genus (r = 0.18-0.48 lineages/myr). The primary shift occurred approximately 4.6 Ma (r = 0.48-1.76) in the montane regions of western North America, followed by a secondary shift approximately 2.7 Ma (r = 0.89-3.33) associated with range expansion and diversification of allopatrically distributed sister clades in the Mexican highlands and Andes. We also recovered evidence for a third independent shift approximately 6.5 Ma at the base of a lower elevation eastern South American grassland and campo rupestre clade (r = 0.36-1.33). Bayesian ancestral state reconstructions and BiSSE likelihood analyses of correlated diversification indicated that increased rates of speciation are strongly associated with the derived evolution of perennial life history and invasion of montane ecosystems. Although we currently lack hard evidence for "replicate adaptive radiations" in the sense of convergent morphological and ecological trajectories among species in different clades, these results are consistent with the hypothesis that iteroparity functioned as an adaptive key innovation, providing a mechanism for range expansion and rapid divergence in upper elevation regions across much of the New World.
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              Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families.

              Although copia retrotransposons are major components of all plant genomes, the evolutionary relationships between individual copia families and between elements from different plant species are only poorly studied. We used 20 copia families from the large-genome plants barley and wheat to identify 46 families of homologous copia elements from rice and 22 from Arabidopsis, two plant species with much smaller genomes. In total, 599 copia elements were analyzed. Phylogenetic analysis showed that copia elements from the four species can be classified into six ancient lineages that existed before the divergence of monocots and dicots. The six lineages show a surprising degree of conservation in sequence organization and other characteristics across species. Additionally, the phylogenetic data suggest at least one case of horizontal gene transfer between the Arabidopsis and rice lineages. Insertion time estimates for 522 high-copy elements showed that retrotransposons from rice were active at different times in waves of activity lasting 0.5-2 million years, depending on the family, whereas elements from wheat and barley had longer periods of activity. We estimated that half of the rice copia elements are truncated or otherwise rearranged after approximately 790,000 yr, which is almost twice the half-life of Arabidopsis elements. In contrast, wheat and barley copia elements appear to have a massively longer half-life, beyond our ability to estimate from the available data. These findings suggest that genome size can be explained by the specific rate of DNA removal from the genome and the length of active periods of retrotransposon families.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                28 July 2016
                2016
                : 7
                : 1152
                Affiliations
                [1] 1Department of Genomics, Institute of Plant Genetics, Polish Academy of Sciences Poznan, Poland
                [2] 2Department of Plant Anatomy and Cytology, University of Silesia in Katowice Katowice, Poland
                Author notes

                Edited by: Changbin Chen, University of Minnesota, USA

                Reviewed by: Mónica Pradillo, Complutense University of Madrid, Spain; Jun Xiao, University of Pennsylvania, USA

                *Correspondence: Karolina Susek ksus@ 123456igr.poznan.pl

                This article was submitted to Plant Science, a section of the journal Frontiers in Plant Science

                †These authors have contributed equally to this work.

                Article
                10.3389/fpls.2016.01152
                4964750
                27516770
                3f45600d-f2bf-49c5-9a29-0106c48ec628
                Copyright © 2016 Susek, Bielski, Hasterok, Naganowska and Wolko.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 February 2016
                : 11 July 2016
                Page count
                Figures: 8, Tables: 2, Equations: 0, References: 58, Pages: 15, Words: 8948
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                polyploidization,evolution,bac-fish,chromosome rearrangement,lupins
                Plant science & Botany
                polyploidization, evolution, bac-fish, chromosome rearrangement, lupins

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