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Genes Duplicated by Polyploidy Show Unequal Contributions to the Transcriptome and Organ-Specific Reciprocal Silencing

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Genes Duplicated by Polyploidy Show Unequal Contributions to the Transcriptome and Organ-Specific Reciprocal Silencing Genes duplicated by polyploidy show unequal SEE COMMENTARY contributions to the transcriptome and organ-specific reciprocal silencing Keith L. Adams*, Richard Cronn†, Ryan Percifield*, and Jonathan F. Wendel*‡ *Department of Botany, Iowa State University, Ames, IA 50011; and †U.S. Department of Agriculture Forest Service, Pacific Northwest Research Station, Corvallis, OR 97331 Communicated by John F. Doebley, University of Wisconsin, Madison, WI, January 31, 2003 (received for review November 20, 2002) Most eukaryotes have genomes that exhibit high levels of gene redundancy, much of which seems to have arisen from one or more cycles of genome doubling. Polyploidy has been particularly promi- nent during flowering plant evolution, yielding duplicated genes (homoeologs) whose expression may be retained or lost either as an immediate consequence of polyploidization or on an evolutionary Fig. 1. Schematic representation of the phylogenetic history of diploid and timescale. Expression of 40 homoeologous gene pairs was assayed by allopolyploid Gossypium. Polyploid formation occurred Ϸ1.5 million years ago cDNA-single-stranded conformation polymorphism in natural (1- to after hybridization between A genome and D genome diploids (19). After 2-million-yr-old) and synthetic tetraploid cotton (Gossypium)tode- formation, the ancestral polyploid radiated into lineages represented now by termine whether homoeologous gene pairs are expressed at equal the five species shown. levels after polyploid formation. Silencing or unequal expression of one homoeolog was documented for 10 of 40 genes examined in ovules of Gossypium hirsutum. Assays of homoeolog expression in 10 transposable elements and other repeated sequences from one organs revealed variable expression levels and silencing, depending genome have colonized the alternative genome subsequent to EVOLUTION on the gene and organ examined. Remarkably, silencing and biased polyploidization (22), whereas other repeated sequences experi- expression of some gene pairs are reciprocal and developmentally enced interlocus homogenization, whereby sequences from one regulated, with one homoeolog showing silencing in some organs genome were overwritten by homoeologous sequences from the and the other being silenced in other organs, suggesting rapid other genome (23). The above studies from Gossypium and other subfunctionalization. Duplicate gene expression was examined in model plant systems highlight the dynamic nature of polyploid additional natural polyploids to characterize the pace at which ex- genomes and the relatively poorly understood and some times pression alteration evolves. Analysis of a synthetic tetraploid re- non-Mendelian mechanisms that often characterize gene and ge- vealed homoeolog expression and silencing patterns that sometimes nome evolution in polyploids (5, 13, 24). mirrored those of the natural tetraploid. Both long-term and imme- Studies of gene expression in natural and synthetic plant diate responses to polyploidization were implicated. Data suggest polyploids have shown that some genes are silenced after that some silencing events are epigenetically induced during the polyploidization, as shown first for isozyme loci (25–27). Ribosomal allopolyploidization process. RNA arrays from one parent may be silenced in some organs (28), although both parental rRNA sets are expressed in floral organs of early all higher eukaryotes have genomes that exhibit extensive Brassica napus (29). Studies of several hundred loci in Arabidopsis Ngene redundancy. Much of this redundancy seems to have suecica and wheat using cDNA-amplified fragment-length poly- arisen from genome doubling, or polyploidy. Polyploidy has been morphism screens have documented silencing of protein coding particularly significant in the evolutionary history of vertebrates genes (30–32). In most cases one homoeolog was silenced, although (1–3), yeast (4), and flowering plants (5–7). Accordingly, most of both homoeologs of some genes were silenced in wheat. these genomes contain duplicated chromosomes or chromosomal To date, relatively little information exists regarding the segments that reflect ancient or recent rounds of polyploidy. proportional contributions of two newly merged genomes to the Polyploidy is especially prevalent in plants, where at least 50% and transcriptome of allopolyploids, both overall and on a gene-by- perhaps up to 95% of angiosperms have experienced one or more gene basis. In part, this absence of evidence reflects experimen- episodes of chromosome doubling in their evolutionary history (8, tal difficulties inherent in distinguishing transcripts from two, 9). Polyploidy is widely perceived to provide raw material for the usually similar parental genomes. Expression of homoeologous origin of physiological and morphological novelty (10, 11). gene pairs has not been compared in different organ types or Investigations of allopolyploid plants (formed from two different between natural and synthetic genotypes. Here, we survey diploids) have shown that the merger of two genomes in a common transcript accumulation for 40 pairs of genes duplicated by nucleus may be accompanied by considerable genomic reorgani- polyploidy (homoeologs) in cotton. Our results show that, al- zation (reviewed in refs. 5, 12, and 13). Rapid and nonrandom though many homoeologs contribute approximately equally to changes, including sequence elimination, have been inferred in the transcriptome, a surprisingly high percentage of genes exhibit wheat and Brassica polyploids (14–18), and these changes may be silencing or biased expression that is developmentally regulated, accompanied by methylation alterations (18). both in natural and synthetic polyploids. We show that in a few Cotton (Gossypium) has been developed as a particularly useful cases alternative homoeologs have been reciprocally silenced in group for studies of polyploidy (19). Polyploidization between an different organs, suggesting subfunctionalization (33, 34). A-genome diploid and a D-genome diploid Ϸ1.5 million years ago (20, 21) created an AD tetraploid lineage that has since diversified into five species, including the commercially important Gossypium Abbreviations: SSCP, single-stranded conformation polymorphism; RT, reverse transcrip- hirsutum (upland cotton) and Gossypium barbadense (Pima cotton) tion; dpa, days postanthesis. (see Fig. 1). Previous studies have demonstrated the possibility of See commentary on page 4369. intergenomic ‘‘cross-talk’’ after polyploid formation. For example, ‡To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0630618100 PNAS ͉ April 15, 2003 ͉ vol. 100 ͉ no. 8 ͉ 4649–4654 Downloaded by guest on September 29, 2021 Materials and Methods Table 1. cDNA-SSCP analysis of homoeolog expression in ovules Plant Materials and Nucleic Acid Extractions. Natural allotetraploids Gene Putative function͞function included G. hirsutum cultivar TM1, Gossypium mustelinum (ac- cession no. AD4-15C), and Gossypium darwinii (accession no. One homoeolog silenced adhE Alcohol dehydrogenase E At only AD5-PW45). Models of their progenitor diploids (19) included Strongly biased expression the A-genome Gossypium herbaceum (accession no. A1-73) and (85͞15% and greater) the D-genome Gossypium raimondii (Wendel laboratory stock). adhD Alcohol dehydrogenase D At Ͼ Dt A synthetic allotetraploid 2(A2D1) was also studied, this gener- G8 Flavonoid 3Ј hydroxylase Dt Ͼ At ated by colchicine-doubling a sterile diploid hybrid formed B5 Oxalate oxidase At Ͼ Dt between the A-genome species Gossypium arboreum and the adhA Alcohol dehydrogenase A Dt Ͼ At D-genome species Gossypium thurberi (35). Because exact pa- Biased expression ͞ ͞ rental plants of this synthetic were not available, G. arboreum (cv. (60 40% to 84 26%) D5 Sugar transporter At Ͼ Dt AKA8401) and G. thurberi (accession nos. 8 and 5) were used as D7 Root hair defective 3 homolog At Ͼ Dt models of the parents. All plants were grown in a greenhouse E6 Potassium transport protein Dt Ͼ At under common conditions. H12 Auxin-alanine hydrolase At Ͼ Dt For RNA isolation, the following vegetative organs were A1520 Unknown Dt Ͼ At collected: young leaves; cotyledons from seedlings 7 days after Equivalent expression first appearance; stems from seedlings after appearance of the 50͞50 to 59͞41% first true leaf; and roots from a mature plant. Floral organs, A6 Unknown collected from multiple plants on the day of anthesis (flower A1751 Subtilisin-like protease opening) between 9:30 a.m. and noon on several days, included B2 Kinesin heavy chain ϩ B3 Enolase bracts (epicalyx), calyx, petals, whole stamens, and stigma B7 Polyubiquitin style (referred to in figures as ‘‘carpels’’). Ovules were col- B8 CAAX-prenyl protease lected at 5, 10, 15, and 20 days postanthesis (dpa) from C1 Vacuolar ATP synthase multiple plants. C3 Syntaxin DNAs were extracted by using the Qiagen (Valencia, CA) C7 Pollen allergen-like protein DNeasy kit. RNAs were extracted as described (36) with a few CesA2 Cellulose synthase modifications (see Supporting Text, which is published as supporting D1 LIM-domain transcription factor Ј Ј information on the PNAS web site, www.pnas.org.). RNA concen- E1 Flavonoid 3 ,5 -hydroxylase E5 Pollen surface protein trations were estimated by using a spectrophotometer. Expression E9 Protein phosphatase assays in ovules used mixed RNAs from 5, 10, 15, and 20 days E11 ␤-D-glucan exohydrolase postanthesis (dpa) in similar amounts. RNAs were treated with F4 Ethylene
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