mRNA and Small RNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation of Allopolyploid Heterosis in Nascent Hexaploid Wheat

Li, Aili; Liu, Dengcai; Wu, Jun; Zhao, Xubo; Hao, Ming; Geng, Shuaifeng; Yan, Jun; Jiang, Xiaoxue; Zhang, Lianquan; Wu, Jinlong; Yin, Lingjie; Zhang, Rongzhi; Wu, Liang; Zheng, Youliang; Mao, Long

doi:10.1105/tpc.114.124388

Cited by 297 publications

(343 citation statements)

References 105 publications

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“…6C). Additional evidence of an Iw2 hairpinforming RNA comes from sRNA sequencing experiments downloaded at the NCBI short-read archive from Li et al (46). Similar to Iw1, the Iw2 region also produces a series of sRNAs, including the most dominant sequence miRW1 (Fig.…”

Section: Expression Of the Mirw1 Precursor In Glaucous Wheat Creates mentioning

confidence: 99%

Long noncoding miRNA gene represses wheat β-diketone waxes

Huang

Feurtado

Smith

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The cuticle of terrestrial plants functions as a protective barrier against many biotic and abiotic stresses. In wheat and other Triticeae, β-diketone waxes are major components of the epicuticular layer leading to the bluish-white glaucous trait in reproductive-age plants. Glaucousness in durum wheat is controlled by a metabolic gene cluster at the WAX1 (W1) locus and a dominant suppressor INHIBITOR of WAX1 (Iw1) on chromosome 2B. The wheat D subgenome from progenitor Aegilops tauschii contains W2 and Iw2 paralogs on chromosome 2D. Here we identify the Iw1 gene from durum wheat and demonstrate the unique regulatory mechanism by which Iw1 acts to suppress a carboxylesterase-like protein gene, W1-COE, within the W1 multigene locus. Iw1 is a long noncoding RNA (lncRNA) containing an inverted repeat (IR) with >80% identity to W1-COE. The Iw1 transcript forms a miRNA precursor-like long hairpin producing a 21-nt predominant miRNA, miRW1, and smaller numbers of related sRNAs associated with the nonglaucous phenotype. When Iw1 was introduced into glaucous bread wheat, miRW1 accumulated, W1-COE and its paralog W2-COE were down-regulated, and the phenotype was nonglaucous and β-diketone-depleted. The IR region of Iw1 has >94% identity to an IR region on chromosome 2 in Ae. tauschii that also produces miRW1 and lies within the marker-based location of Iw2. We propose the Iw loci arose from an inverted duplication of W1-COE and/or W2-COE in ancestral wheat to form evolutionarily young miRNA genes that act to repress the glaucous trait.glaucous | inhibitor of wax | small RNA | long noncoding RNA | WAX1 P lant epicuticular waxes deposited on the outer surface of the plant cuticle produce a water-resistant layer that serves to reduce nonstomatal water loss and mitigate the effects of heat and UV radiation as well as pathogen and insect attacks (1). Grasses in the Triticeae tribe, subfamily Pooideae, which include the cultivated species barley (Hordeum vulgare; 2n = 2x = 14), rye (Secale cereale, 2n = 2x = 14), durum wheat (Triticum durum; 2n = 4x = 28, AABB), and bread wheat (Triticum aestivum; 2n = 6x = 42, AABBDD), have two predominant pathways for wax production: (i) an alcohol-and alkane-rich wax pathway and (ii) a pathway leading to β-diketones and derivatives including hydroxy-β-diketones (2). The alcohol and alkane waxes are prevalent in earlier development and on leaves, whereas β-diketones dominate during the reproductive phase, particularly on leaf sheaths and flower heads (3, 4). β-Diketone wax is predominantly hentriacontane-14, 16-dione, which consists of a 31-carbon chain with carbonyl groups at C 14 and C 16 . In durum wheat, about 20% of the β-diketone is hydroxylated to form 25-hydroxy-β-diketone, whereas in bread wheat hydroxylation is at C 8 or C 9 (5). β-Diketone wax deposition manifests visibly as glaucousness, a bluish-white coloration on stems, leaves, and flower heads. However, the relationship between a glaucous appearance and the total amount of cuticular wax can be inconsistent, especially during t...

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Section: Expression Of the Mirw1 Precursor In Glaucous Wheat Creates mentioning

confidence: 99%

Long noncoding miRNA gene represses wheat β-diketone waxes

Huang

Feurtado

Smith

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…2); this occurred irrespective of whether they were produced by the crossing of unreduced gametes of tetraploids or by the colchicine treatment-induced chromosome doubling of hybridized triploids (Tanaka, 1961). This maternal expression dominance has been reported in wheat Li et al, 2014) and other plants such as Spartina species (Chelaifa et al, 2010).…”

Section: Discussionmentioning

confidence: 93%

“…Persistent NEGs are NEGs that are commonly detected during nascent allopolyploidization and they seem to characterize the phenotypes of allohexaploid wheat (Li et al, 2014); thus, heritable NEGs were selected from the NEGs detected in S 0 , S 1 and S 5 /S 14 of the two combinations of allopolyploid wheats (Fig. 4 and Supplementary Table S2).…”

Section: Non-additively Expressed Genes During the Course Of Allopolymentioning

confidence: 99%

Comparison of genome-wide gene expression patterns in the seedlings of nascent allohexaploid wheats produced by two combinations of hybrids

et al. 2015

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Allopolyploidization in plants is an important event that enhances heterosis and environmental adaptation. Common wheat, Triticum aestivum (AABBDD), which is an allohexaploid that evolved from an allopolyploidization event between T. turgidum (AABB) and Aegilops tauschii (DD), shows more growth vigor and wider adaptation than tetraploid wheats. To better understand the molecular basis for the heterosis of hexaploid wheat, we systematically analyzed the genomewide gene expression patterns of two combinations of newly hybridized triploids (ABD), their chromosome-doubled hexaploids (AABBDD), stable synthetic hexaploids (AABBDD) and natural hexaploids, in addition to their parents, T. turgidum (AABB) and Ae. tauschii (DD), using a microarray to reconstruct the events of allopolyploidization and genome stabilization. Overall comparisons of gene expression profiles showed that the newly generated hexaploids exhibited gene expression patterns similar to those of their maternal tetraploids, irrespective of hybrid combination. With successive generations, the gene expression profiles of nascent hexaploids became less similar to the maternal profiles, and belonged to a separate cluster from the natural hexaploids. Triploids revealed characteristic expression patterns, suggesting endosperm effects. In the newly hybridized triploids (ABD) of two independent synthetic lines, approximately onefifth of expressed genes displayed non-additive expression; the number of these genes decreased with polyploidization and genome stabilization. Approximately 20% of the non-additively expressed genes were transmitted across generations throughout allopolyploidization and successive self-pollinations, and 43 genes overlapped between the two combinations, indicating that shared gene expression patterns can be seen during allohexaploidization. Furthermore, four of these 43 genes were involved in starch and sucrose metabolism, suggesting that these metabolic events play key roles in the hybrid vigor of hexaploid wheat.

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“…As these allopolyploids experienced the evolutionary history of thousands or millions of years, their component genomes diverged from those of the extant descendants of their progenitors (Brenchley et al 2012;Paterson et al 2012;Chalhoub et al 2014;Li et al 2014;Zhang et al 2015b). The extent and pattern of the genomic changes seemed to be affected by age, genome relatedness, and existence or absence of the genetic system regulating the chromosome pairing, such as the Ph1 loci in wheat.…”

mentioning

confidence: 99%

“…For the small and similar size of the chromosomes (Prakash 2009;Heneen et al 2012) and the later development of chromosomespecific cytological markers (Xiong and Pires 2011), the dissection of the A and C genomes in natural B. napus was not achieved by the development of the complete set of additions. One nullisomic of B. napus with the loss of the C2 chromosome established up to now showed much reduced plant stature and shorter growth period and also the genomewide change of gene expression (Zhu et al 2015).As these allopolyploids experienced the evolutionary history of thousands or millions of years, their component genomes diverged from those of the extant descendants of their progenitors (Brenchley et al 2012;Paterson et al 2012;Chalhoub et al 2014;Li et al 2014;Zhang et al 2015b). The extent and pattern of the genomic changes seemed to be affected by age, genome relatedness, and existence or absence of the genetic system regulating the chromosome pairing, such as the Ph1 loci in wheat.…”

mentioning

confidence: 99%

Extraction of the Constituent Subgenomes of the Natural Allopolyploid Rapeseed (Brassica napus L.)

Zhu

Zeng

et al. 2016

Genetics

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As the dynamic nature of progenitor genomes accompanies the speciation by interspecific hybridization, the extraction of the constituent subgenome(s) from a natural allopolyploid species of long history and then restitution of the progenitor(s) provides the unique opportunity to study the genome evolution and interplay. Herein, the A subgenome from the allotetraploid oilseed rape (Brassica napus L., AACC) was extracted through inducing the preferential elimination of C-subgenome chromosomes in intertribal crosses and the progenitor B. rapa was restituted (RBR). Then by crossing and backcrossing RBR with B. napus donor, the C subgenome was in situ dissected by adding each of its nine chromosomes to the extracted A subgenome and establishing the whole set of monosonic alien addition lines (MAALs). RBR from spring-type B. napus genotype "Oro" expressed a phenotype resembling some type of B. rapa never observed before, but showed a winter-type flowering habit. This RBR had weaker growth vigor and suffered more seriously from biotic and abiotic stresses compared with Oro. The phenotypes specific for these MAALs showed the location of the related genes on the particular C-subgenome chromosomes. These MAALs exhibited obviously different frequencies in homeologous pairing and transmission of additional C-subgenome chromosomes, which were associated with the distinct degrees of their relatedness, and even with the possible genetic regulation for meiotic pairing evolved in B. napus. Finally, large scaffolds undetermined for sequence assembly of B. napus were anchored to specific C-subgenome chromosomes using MAALs.KEYWORDS allopolyploid; Brassica napus; B. rapa; alien additional lines; aneuploid M ANY angiosperms including important crops (bread wheat, cotton, oilseed rape, tobacco, etc.) are allopolyploid species that originated from interspecific hybridizations between two or more diploid ancestors followed by chromosome doubling (Ramsey and Schemske 1998;Levin 2003;Otto 2007;Doyle et al. 2008;Soltis and Soltis 2012). These allopolyploid crops outcompete their progenitors by their adaptability to a wide range of climatic conditions and higher yield and better quality of targeted products, under human domestication and improvement. To unravel the origin and structure of the component genomes in these crops has been the goal of the extensive genetic research over a long period. The hybridization events leading to the evolutionary origin of these allopolyploids were traditionally elucidated by the artificial synthesis of their counterparts from the crosses between the extant relatives of the presumed progenitors available or by observing the meiotic chromosome pairing in the hybrids between the natural allopolyploid and the possible progenitors (Kihara 1924;Nagaharu 1935). Alternatively, the genome of one progenitor (AA) was readily dissected by separating and adding its own chromosome to the genome of another progenitor (BB) (namely the alien addition lines), from successively backcrossing the natural or synthesi...

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mRNA and Small RNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation of Allopolyploid Heterosis in Nascent Hexaploid Wheat

Cited by 297 publications

References 105 publications

Long noncoding miRNA gene represses wheat β-diketone waxes

Long noncoding miRNA gene represses wheat β-diketone waxes

Comparison of genome-wide gene expression patterns in the seedlings of nascent allohexaploid wheats produced by two combinations of hybrids

Extraction of the Constituent Subgenomes of the Natural Allopolyploid Rapeseed (Brassica napus L.)

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