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      QTL Analysis for Transgressive Resistance to Root-Knot Nematode in Interspecific Cotton ( Gossypium spp.) Progeny Derived from Susceptible Parents

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          Abstract

          The southern root-knot nematode (RKN, Meloidogyne incognita) is a major soil-inhabiting plant parasite that causes significant yield losses in cotton ( Gossypium spp.). Progeny from crosses between cotton genotypes susceptible to RKN produced segregants in subsequent populations which were highly resistant to this parasite. A recombinant inbred line (RIL) population of 138 lines developed from a cross between Upland cotton TM-1 ( G. hirsutum L.) and Pima 3–79 ( G. barbadense L.), both susceptible to RKN, was used to identify quantitative trait loci (QTLs) determining responses to RKN in greenhouse infection assays with simple sequence repeat (SSR) markers. Compared to both parents, 53.6% and 52.1% of RILs showed less ( P<0.05) root-galling index (GI) and had lower ( P<0.05) nematode egg production (eggs per gram root, EGR). Highly resistant lines (transgressive segregants) were identified in this RIL population for GI and/or EGR in two greenhouse experiments. QTLs were identified using the single-marker analysis nonparametric mapping Kruskal-Wallis test. Four major QTLs located on chromosomes 3, 4, 11, and 17 were identified to account for 8.0 to 12.3% of the phenotypic variance ( R 2 ) in root-galling. Two major QTLs accounting for 9.7% and 10.6% of EGR variance were identified on chromosomes 14 and 23 ( P<0.005), respectively. In addition, 19 putative QTLs ( P<0.05) accounted for 4.5–7.7% of phenotypic variance ( R 2 ) in GI, and 15 QTLs accounted for 4.2–7.3% of phenotypic variance in EGR. In lines with alleles positive for resistance contributed by both parents in combinations of two to four QTLs, dramatic reductions of >50% in both GI and EGR were observed. The transgressive segregants with epistatic effects derived from susceptible parents indicate that high levels of nematode resistance in cotton may be attained by pyramiding positive alleles using a QTL mapping approach.

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          Transgressive segregation, adaptation and speciation.

          The production of extreme or 'transgressive' phenotypes in segregating hybrid populations has been speculated to contribute to niche divergence of hybrid lineages. Here, we assess the frequency of transgressive segregation in hybrid populations, describe its genetic basis and discuss the factors that best predict its occurrence. From a survey of 171 studies that report phenotypic variation in segregating hybrid populations, we show that transgression is the rule rather than the exception. In fact, 155 of the 171 studies (91%) report at least one transgressive trait, and 44% of 1229 traits examined were transgressive. Transgression occurred most frequently in intraspecific crosses involving inbred, domesticated plant populations, and least frequently in interspecific crosses between outbred, wild animal species. Quantitative genetic studies of plant hybrids consistently point to the action of complementary genes as the primary cause of transgression, although overdominance and epistasis also contribute. Complementary genes appear to be common for most traits, with the possible exception of those with a history of disruptive selection. These results lend credence to the view that hybridization may provide the raw material for rapid adaptation and provide a simple explanation for niche divergence and phenotypic novelty often associated with hybrid lineages.
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            The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations.

            Segregating hybrids often exhibit phenotypes that are extreme or novel relative to the parental lines. This phenomenon is referred to as transgressive segregation, and it provides a mechanism by which hybridization might contribute to adaptive evolution. Genetic studies indicate that transgressive segregation typically results from recombination between parental taxa that possess quantitative trait loci (QTLs) with antagonistic effects (i.e. QTLs with effects that are in the opposite direction to parental differences for those traits). To assess whether this genetic architecture is common, we tabulated the direction of allelic effects for 3252 QTLs from 749 traits and 96 studies. Most traits (63.6%) had at least one antagonistic QTL, indicating that the genetic substrate for transgressive segregation is common. Plants had significantly more antagonistic QTLs than animals, which agrees with previous reports that transgressive segregation is more common in plants than in animals. Likewise, antagonistic QTLs were more frequent in intra- than in interspecific crosses and in morphological than in physiological traits. These results indicate that transgressive segregation provides a general mechanism for the production of extreme phenotypes at both above and below the species level and testify to the possible creative part of hybridization in adaptive evolution and speciation.
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              QTL analysis of transgressive segregation in an interspecific tomato cross.

              Two accessions, representing the species Lycopersicon esculentum (cultivated tomato) and Lycopersicon pennellii (a wild relative), were evaluated for 11 quantitative traits and found to be significantly different for 10 of the traits. Transgressive segregation was observed for eight of the traits in a large interspecific F2 population. When restriction fragment length polymorphism markers were used as probes for the quantitative trait loci (QTL) underlying the traits, 74 significant QTL (LOD > 2) were detected. Thirty-six percent of those QTL had alleles with effects opposite to those predicted by the parental phenotypes. These QTL were directly related to the appearance of transgressive individuals in the F2 for those traits which showed transgressive segregation. However, the same types of QTL (with allelic effects opposite to those predicted by the parents) were also observed for traits that did not display transgressive segregation in the F2. One such trait was dry weight accumulation. When two overdominant QTL (detected in the F2) for this trait were backcrossed into the L. esculentum genetic background, transgressive individuals were recovered and their occurrence was associated with the two QTL demonstrating the potential for transgressive segregation for all characters and implicating overdominance as a second cause of transgressive segregation. Epistasis was not implicated in transgressive segregation in either the F2 or backcross generations. Results from this research not only reveal the basis of wide-cross transgressive segregation, but demonstrate that molecular markers can be used to identify QTL (from wild species) responsible for transgressive phenotypes and to selectively transfer them into crop species. This strategy might be used to improve many traits of economic importance including those for which wild species appear phenotypically inferior to their cultivated counterparts.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                13 April 2012
                : 7
                : 4
                : e34874
                Affiliations
                [1 ]Department of Nematology, University of California Riverside, Riverside, California, United States of America
                [2 ]United States Department of Agriculture-Agricultural Research Service, Western Integrated Cropping Systems Research Unit, Shafter, California, United States of America
                [3 ]United States Department of Agriculture-Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, Texas, United States of America
                East Carolina University, United States of America
                Author notes

                Conceived and designed the experiments: PAR CW MU. Performed the experiments: PAR CW MU TM. Analyzed the data: PAR CW MU TM JZY. Contributed reagents/materials/analysis tools: PAR CW MU TM. Wrote the paper: PAR CW MU.

                Article
                PONE-D-11-17655
                10.1371/journal.pone.0034874
                3325951
                22514682
                4063fcaa-1032-4c5d-97e2-93268dd1862d
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 7 September 2011
                : 10 March 2012
                Page count
                Pages: 9
                Categories
                Research Article
                Agriculture
                Agricultural Biotechnology
                Marker-Assisted Selection
                Crops
                Fibers
                Cotton
                Biology
                Computational Biology
                Genomics
                Genome Analysis Tools
                Trait Locus Analysis
                Plant Science
                Plant Evolution
                Plant Genetics
                Plant Genomics
                Plant Pathology

                Uncategorized
                Uncategorized

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