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      Physical and Genetic Structure of the Maize Genome Reflects Its Complex Evolutionary History

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          Abstract

          Maize (Zea mays L.) is one of the most important cereal crops and a model for the study of genetics, evolution, and domestication. To better understand maize genome organization and to build a framework for genome sequencing, we constructed a sequence-ready fingerprinted contig-based physical map that covers 93.5% of the genome, of which 86.1% is aligned to the genetic map. The fingerprinted contig map contains 25,908 genic markers that enabled us to align nearly 73% of the anchored maize genome to the rice genome. The distribution pattern of expressed sequence tags correlates to that of recombination. In collinear regions, 1 kb in rice corresponds to an average of 3.2 kb in maize, yet maize has a 6-fold genome size expansion. This can be explained by the fact that most rice regions correspond to two regions in maize as a result of its recent polyploid origin. Inversions account for the majority of chromosome structural variations during subsequent maize diploidization. We also find clear evidence of ancient genome duplication predating the divergence of the progenitors of maize and rice. Reconstructing the paleoethnobotany of the maize genome indicates that the progenitors of modern maize contained ten chromosomes.

          Author Summary

          As a cash crop and a model biological system, maize is of great public interest. To facilitate maize molecular breeding and its basic biology research, we built a high-resolution physical map with two different fingerprinting methods on the same set of bacterial artificial chromosome clones. The physical map was integrated to a high-density genetic map and further serves as a framework for the maize genome-sequencing project. Comparative genomics showed that the euchromatic regions between rice and maize are very conserved. Physically we delimited these conserved regions and thus detected many genome rearrangements. We defined extensively the duplication blocks within the maize genome. These blocks allowed us to reconstruct the chromosomes of the maize progenitor. We detected that maize genome has experienced two rounds of genome duplications, an ancient one before maize–rice divergence and a recent one after tetraploidization.

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          Most cited references48

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          Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.

          Integration of structural genomic data from a largely assembled rice genome sequence, with phylogenetic analysis of sequence samples for many other taxa, suggests that a polyploidization event occurred approximately 70 million years ago, before the divergence of the major cereals from one another but after the divergence of the Poales from the Liliales and Zingiberales. Ancient polyploidization and subsequent "diploidization" (loss) of many duplicated gene copies has thus shaped the genomes of all Poaceae cereal, forage, and biomass crops. The Poaceae appear to have evolved as separate lineages for approximately 50 million years, or two-thirds of the time since the duplication event. Chromosomes that are predicted to be homoeologs resulting from this ancient duplication event account for a disproportionate share of incongruent loci found by comparison of the rice sequence to a detailed sorghum sequence-tagged site-based genetic map. Differential gene loss during diploidization may have contributed many of these incongruities. Such predicted homoeologs also account for a disproportionate share of duplicated sorghum loci, further supporting the hypothesis that the polyploidization event was common to sorghum and rice. Comparative gene orders along paleo-homoeologous chromosomal segments provide a means to make phylogenetic inferences about chromosome structural rearrangements that differentiate among the grasses. Superimposition of the timing of major duplication events on taxonomic relationships leads to improved understanding of comparative gene orders, enhancing the value of data from botanical models for crop improvement and for further exploration of genomic biodiversity. Additional ancient duplication events probably remain to be discovered in other angiosperm lineages.
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            Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat.

            The foundation of western civilization owes much to the high fertility of bread wheat, which results from the stability of its polyploid genome. Despite possessing multiple sets of related chromosomes, hexaploid (bread) and tetraploid (pasta) wheat both behave as diploids at meiosis. Correct pairing of homologous chromosomes is controlled by the Ph1 locus. In wheat hybrids, Ph1 prevents pairing between related chromosomes. Lack of Ph1 activity in diploid relatives of wheat suggests that Ph1 arose on polyploidization. Absence of phenotypic variation, apart from dosage effects, and the failure of ethylmethane sulphonate treatment to yield mutants, indicates that Ph1 has a complex structure. Here we have localized Ph1 to a 2.5-megabase interstitial region of wheat chromosome 5B containing a structure consisting of a segment of subtelomeric heterochromatin that inserted into a cluster of cdc2-related genes after polyploidization. The correlation of the presence of this structure with Ph1 activity in related species, and the involvement of heterochromatin with Ph1 (ref. 6) and cdc2 genes with meiosis, makes the structure a good candidate for the Ph1 locus.
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              Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome.

              Long terminal repeat (LTR) retrotransposons have been shown to make up much of the maize genome. Although these elements are known to be prevalent in plant genomes of a middle-to-large size, little information is available on the relative proportions composed by specific families of elements in a single genome. We sequenced a library of randomly sheared genomic DNA from maize to characterize this genome. BLAST analysis of these sequences demonstrated that the maize genome is composed of diverse sequences that represent numerous families of retrotransposons. The largest families contain the previously described elements Huck, Ji, and Opie. Approximately 5% of the sequences are predicted to encode proteins. The genomic abundance of 16 families of elements was estimated by hybridization to an array of 10,752 maize bacterial artificial chromosome (BAC) clones. Comparisons of the number of elements present on individual BACs indicated that retrotransposons are in general randomly distributed across the maize genome. A second library was constructed that was selected to contain sequences hypomethylated in the maize genome. Sequence analysis of this library indicated that retroelements abundant in the genome are poorly represented in hypomethylated regions. Fifty-six retroelement sequences corresponding to the integrase and reverse transcriptase domains were isolated from approximately 407,000 maize expressed sequence tags (ESTs). Phylogenetic analysis of these and the genomic retroelement sequences indicated that elements most abundant in the genome are less abundant at the transcript level than are more rare retrotransposons. Additional phylogenies also demonstrated that rice and maize retrotransposon families are frequently more closely related to each other than to families within the same species. An analysis of the GC content of the maize genomic library and that of maize ESTs did not support recently published data that the gene space in maize is found within a narrow GC range, but does indicate that genic sequences have a higher GC content than intergenic sequences (52% vs. 47% GC).
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                pgen
                plge
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                July 2007
                20 July 2007
                12 June 2007
                : 3
                : 7
                : e123
                Affiliations
                [1 ] Arizona Genomics Institute, University of Arizona, Tucson, Arizona, United States of America
                [2 ] Department of Plant Sciences, University of Arizona, Tucson, Arizona, United States of America
                [3 ] BIO5 Institute, University of Arizona, Tucson, Arizona, United States of America
                [4 ] Division of Plant Sciences, University of Missouri, Columbia, Missouri, United States of America
                [5 ] Plant Genetics Research Unit, Agricultural Research Service, United States Department of Agriculture, Columbia, Missouri, United States of America
                [6 ] Arizona Genomics Computational Laboratory, University of Arizona, Tucson, Arizona, United States of America
                [7 ] Plant Genome Initiative at Rutgers, Waksman Institute, Rutgers, The State University of New Jersey, Piscataway, New Jersey, United States of America
                [8 ] Plant Genome Mapping Laboratory, Departments of Crop and Soil Science, Plant Biology, and Genetics, University of Georgia, Athens, Georgia, United States of America
                [9 ] Division of Biological Sciences, University of Missouri, Columbia, Missouri, Arizona, United States of America
                The Salk Institute for Biological Studies, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: cari@ 123456agcol.arizona.edu (CS); rwing@ 123456ag.arizona.edu (RAW)
                Article
                07-PLGE-RA-0126R2 plge-03-07-11
                10.1371/journal.pgen.0030123
                1934398
                17658954
                557b71a3-2adc-49c4-bbfc-b0746ae6da8f
                Copyright: © 2007 This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 22 February 2007
                : 11 June 2007
                Page count
                Pages: 10
                Categories
                Research Article
                Genetics and Genomics
                Genetics and Genomics
                Genetics and Genomics
                Genetics and Genomics
                Eukaryotes
                Plants
                Zea
                Custom metadata
                Wei F, Coe E, Nelson W, Bharti AK, Engler F, et al. (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3(7): e123. doi: 10.1371/journal.pgen.0030123

                Genetics
                Genetics

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