The<i>Populus</i>Class III HD ZIP,<i>popREVOLUTA</i>, Influences Cambium Initiation and Patterning of Woody Stems

Robischon, Marcel; Du, Juan; Miura, Eriko; Groover, Andrew

doi:10.1104/pp.110.167007

Cited by 166 publications

(138 citation statements)

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“…Among many SNP-trait associations, these studies revealed genetic associations of wood cellulose content and leaf phenology traits with SNPs in noncoding regions of distinct splice variants of the poplar REV gene Potri.009G014500 (PtREV; Fig. 1; Table I), consistent with fundamental functions for REV in regulating the architecture of leaf and vascular systems (Zhong et al, 1997;Otsuga et al, 2001;Emery et al, 2003;Robischon et al, 2011;Stirnberg et al, 2012). An additional putatively functional polymorphism common to all splice variants of REV is associated with Melampsora spp.…”

Section: Resultsmentioning

confidence: 93%

“…In particular, REV (synonymous with INTERFASCICULAR FBERLESS1 and AMPHIVASAL VASCULAR BUNDLES1 [AVB1]), encoding one of five Arabidopsis (Arabidopsis thaliana) class III HD ZIP transcription factors, regulates meristem function, polarity of lateral organs, vascular architecture and development, and interfascicular fiber differentiation in Arabidopsis and other angiosperms Ratcliffe et al, 2000, Emery et al, 2003Zhong and Ye, 2004). In poplar, the REV ortholog PtREV influences cambium initiation and patterning of woody stems (Robischon et al, 2011;Hu et al, 2012). REV is part of a complex regulatory system involving auxin, KANADI (KAN1) transcription factors, and miRNA (Emery et al, 2003;Ilegems et al, 2010;Brandt et al, 2012;Schuetz et al, 2013).…”

Section: Resultsmentioning

confidence: 99%

“…The class III homeodomain leucine zipper (HD ZIP) gene REVOLUTA (REV) is involved in auxin-mediated adaxial-abaxial patterning of plant leaves in general and patterning of secondary vascular tissues in woody species in particular (Emery et al, 2003;Robischon et al, 2011) and represents an interesting example of how phenotypic variation can be mediated through interference with microRNA (miRNA) binding rather than nonsynonymous mutations in the coding sequence (Emery et al, 2003;Ong and Wickneswari, 2012). Here, we discuss specific results obtained from genotype-phenotype association studies in poplar (Populus trichocarpa; La Mantia et al, 2013;Porth et al, 2013a;A.D.…”

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confidence: 99%

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Extensive Functional Pleiotropy ofREVOLUTASubstantiated through Forward Genetics

et al. 2013

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In plants, genes may sustain extensive pleiotropic functional properties by individually affecting multiple, distinct traits. We discuss results from three genome-wide association studies of approximately 400 natural poplar (Populus trichocarpa) accessions phenotyped for 60 ecological/biomass, wood quality, and rust fungus resistance traits. Single-nucleotide polymorphisms (SNPs) in the poplar ortholog of the class III homeodomain-leucine zipper transcription factor gene REVOLUTA (PtREV) were significantly associated with three specific traits. Based on SNP associations with fungal resistance, leaf drop, and cellulose content, the PtREV gene contains three potential regulatory sites within noncoding regions at the gene's 39 end, where alternative splicing and messenger RNA processing actively occur. The polymorphisms in this region associated with leaf abscission and cellulose content are suggested to represent more recent variants, whereas the SNP associated with leaf rust resistance may be more ancient, consistent with REV's primary role in auxin signaling and its functional evolution in supporting fundamental processes of vascular plant development.

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Section: Resultsmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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Extensive Functional Pleiotropy ofREVOLUTASubstantiated through Forward Genetics

et al. 2013

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“…In a recent study using Acacia mangium as lignification model system, the conserved miR166 was shown to be strongly down-regulated in xylem when compared to phloem, suggesting its potential role in xylem development by indirect regulation of the genes involved in lignin biosynthesis (Ong and Wickneswari 2012). Transgenic Populus expressing a miR166 resistant target gene have developed phenotypic abnormalities affecting the primary and secondary growth, including the abnormal formation of cambia within cortical parenchyma that can produce secondary vascular tissues in reverse polarity (Robischon et al 2011). More recently, Puzey et al (2012) identified several xylem-enriched miRNAs predicted to target genes known to be important in secondary growth, including xyloglucan endotransglycosylase/hydrolase and vascular-related transcription factors (Puzey et al 2012).…”

Section: Introductionmentioning

confidence: 99%

miRNA profiling in leaf and cork tissues of Quercus suber reveals novel miRNAs and tissue-specific expression patterns

Chaves

Lin

Pinto-Ricardo

et al. 2014

Tree Genetics & Genomes

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The differentiation of cork (phellem) cells from the phellogen (cork cambium) is a secondary growth process observed in the cork oak tree conferring a unique ability to produce a thick layer of cork. At present, the molecular regulators of phellem differentiation are unknown. The previously documented involvement of microRNAs in the regulation of developmental processes, including secondary growth, motivated the search for these regulators in cork oak tissues.We performed deep-sequencing of the small-RNA fraction obtained from cork oak leaves and differentiating phellem. RNA sequences with lengths of 19-25 nt derived from the two libraries were analysed, leading to the identification of 41 families of conserved miRNAs, of which the most abundant were miR167, miR165/166, miR396 and miR159. Thirty novel miRNA candidates were also unveiled, 11 of which were unique to leaves and 13 to phellem. Northern blot detection of a set of conserved and novel-miRNAs confirmed their differential expression profile. Prediction and analysis of putative miRNA target genes provided clues regarding processes taking place in leaf and phellem tissues but further experimental work will be needed for functional characterization. In conclusion, we here provide a first characterization of the miRNA population in a Fagacea species and the comparative analysis of miRNA expression in leaf and phellem libraries represents an important step to uncovering specific regulatory networks controlling phellem differentiation.

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“…However, few studies have explored the potential impact of miRNAs during the growth of longlived perennial plants (Robischon et al, 2011;Lu et al, 2013). Recently, several studies have used reverse genetics on woody plants to reveal the biological importance of miRNA-target interactions in tree growth and wood formation (Robischon et al, 2011;Lu et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Dissection of allelic interactions among Pto-miR257 and its targets and their effects on growth and wood properties in Populus

Chen

et al. 2016

Heredity

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MicroRNAs (miRNAs) have important roles in the regulation of genes; however, for trees few studies have explored the potential impact of the interactions between miRNAs and their target genes. Here, we performed transcript profiling and association genetics (single-SNP, haplotype-based and multi-SNP associations) to study the genetic regulatory relationship of Pto-miR257 and its 12 target genes in 435 individuals of a natural population of Populus tomentosa. Expression profiling of Pto-miR257 and its targets showed a negative relationship between their expression levels. Of the 61 single-nucleotide polymorphisms (SNPs) detected in Pto-miR257, 6 in the pre-mature region strongly affected its secondary stability and 1 in the mature region could alter its target spectrum. Among the 1029 SNPs in the targets, 3 were located in target sites that could change the binding affinity of Pto-miR257. Single-SNP association analysis revealed that SNPs in Pto-miR257 and target genes associated with both growth and wood property traits, in agreement with haplotype-based identifications. Multi-SNP association found that 10 targets shared at least one common trait with Pto-miR257, with phenotypic variance from 0.5 to 8.5%, suggesting a possible internal genetic interaction between them. Epistasis analysis showed significant epistatic interactions among Pto-miR257 and its targets. Therefore, our study demonstrated Pto-miR257 and its 12 targets had roles in wood formation and revealed the genetic interaction network between the miRNA and its targets under additive, dominant and epistatic models. Thus, association genetics can be used to decipher the interactions between miRNAs and their target genes and to help understand the genetic architecture of complex traits.

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ThePopulusClass III HD ZIP,popREVOLUTA, Influences Cambium Initiation and Patterning of Woody Stems

Cited by 166 publications

References 57 publications

Extensive Functional Pleiotropy ofREVOLUTASubstantiated through Forward Genetics

Extensive Functional Pleiotropy ofREVOLUTASubstantiated through Forward Genetics

miRNA profiling in leaf and cork tissues of Quercus suber reveals novel miRNAs and tissue-specific expression patterns

Dissection of allelic interactions among Pto-miR257 and its targets and their effects on growth and wood properties in Populus

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