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The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems.

Du J, Miura E, Robischon M, Martinez C, Groover A - PLoS ONE (2011)

Bottom Line: Synthetic miRNA knock down of POPCORONA results in abnormal lignification in cells of the pith, while overexpression of a miRNA-resistant POPCORONA results in delayed lignification of xylem and phloem fibers during secondary growth.POPCORONA misexpression also results in coordinated changes in expression of genes within a previously described transcriptional network regulating cell differentiation and cell wall biosynthesis, and hormone-related genes associated with fiber differentiation.POPCORONA illustrates another function of Class III HD ZIPs: regulating cell differentiation during secondary growth.

View Article: PubMed Central - PubMed

Affiliation: Institute of Forest Genetics, Pacific Southwest Research Station, U.S. Forest Service, Davis, California, United States of America.

ABSTRACT
The developmental mechanisms regulating cell differentiation and patterning during the secondary growth of woody tissues are poorly understood. Class III HD ZIP transcription factors are evolutionarily ancient and play fundamental roles in various aspects of plant development. Here we investigate the role of a Class III HD ZIP transcription factor, POPCORONA, during secondary growth of woody stems. Transgenic Populus (poplar) trees expressing either a miRNA-resistant POPCORONA or a synthetic miRNA targeting POPCORONA were used to infer function of POPCORONA during secondary growth. Whole plant, histological, and gene expression changes were compared for transgenic and wild-type control plants. Synthetic miRNA knock down of POPCORONA results in abnormal lignification in cells of the pith, while overexpression of a miRNA-resistant POPCORONA results in delayed lignification of xylem and phloem fibers during secondary growth. POPCORONA misexpression also results in coordinated changes in expression of genes within a previously described transcriptional network regulating cell differentiation and cell wall biosynthesis, and hormone-related genes associated with fiber differentiation. POPCORONA illustrates another function of Class III HD ZIPs: regulating cell differentiation during secondary growth.

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Phylogenetic relationships among Class III HD ZIP gene family in land plants determined using maximum parsimony analysis.Bootstrap support values above 50% are presented above branches and Bayesian support values above 0.50 are presented below branches, where * indicates maximum 1.00 support. Black squares indicate major duplication events, while the empty square represents evidence of a duplication event without bootstrap support. Major clades are presented by longitudinal lines to the right of the tree, where solid lines represent fully supported monophyletic clades (PHB, C8, and CNA) and dashed lines indicate clade supported by Bayesian, but not bootstrap support. Black triangles represent where the AtHB8, AlHB8, MgHB7 clade is supported according to Bayesian analysis. Species abbreviations: At, Arabidopsis thaliana; Bd, Brachypodium distachyon; Al, Arabidopsis lyrata; Cp, Carica papaya; Cs, Cucumis sativus; Gm, Glycine max; Me, Manihot esculenta; Mt, Medicago truncatula; Mg, Mimulus guttatus; Os, Oryzas sativa; Pt, Populus trichocarpa; Pp, Physcomitrella patens; Rc, Ricinus communis; Sm, Selanginella moellendorffii, Sb, Sorghum bicolor; Vv, Vitis vinifera; Zm, Zea mays.
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pone-0017458-g001: Phylogenetic relationships among Class III HD ZIP gene family in land plants determined using maximum parsimony analysis.Bootstrap support values above 50% are presented above branches and Bayesian support values above 0.50 are presented below branches, where * indicates maximum 1.00 support. Black squares indicate major duplication events, while the empty square represents evidence of a duplication event without bootstrap support. Major clades are presented by longitudinal lines to the right of the tree, where solid lines represent fully supported monophyletic clades (PHB, C8, and CNA) and dashed lines indicate clade supported by Bayesian, but not bootstrap support. Black triangles represent where the AtHB8, AlHB8, MgHB7 clade is supported according to Bayesian analysis. Species abbreviations: At, Arabidopsis thaliana; Bd, Brachypodium distachyon; Al, Arabidopsis lyrata; Cp, Carica papaya; Cs, Cucumis sativus; Gm, Glycine max; Me, Manihot esculenta; Mt, Medicago truncatula; Mg, Mimulus guttatus; Os, Oryzas sativa; Pt, Populus trichocarpa; Pp, Physcomitrella patens; Rc, Ricinus communis; Sm, Selanginella moellendorffii, Sb, Sorghum bicolor; Vv, Vitis vinifera; Zm, Zea mays.

Mentions: The POPCORONA (PCN) gene (also called Pt-ATHB.12; Joint Genome Institute Populus v.1.1 gene model fgenesh4_pm.C_LG_I000560; Phytozome Populus v2.0 gene model POPTR_0001s18930: GenBank XM_002299699) was amplified from cDNA of the sequenced Populus trichocarpa individual [33] based on similarity to the Arabidopsis thaliana ATHB15/CORONA (Materials and Methods). To determine the relationship of PCN to other Class III HD ZIPs, a phylogenetic analysis of Class III HD ZIP sequences from whole-genome sequencing projects was undertaken (Materials and Methods). Maximum parsimony analysis from the nucleotide sequence alignment of the coding sequences of Class III HD ZIPs found in 17 plant species and deduced from amino acid sequence alignments yielded a single tree, with clade support from Bayesian and bootstrap analysis (Fig. 1). Sequences from Physcomitrella patens, a moss, were used as outgroups to root the tree. Sequences from the lycophyte representative, Selanginella moellendorffii, formed a clade (53% bootstrap, 1.00 Bayesian) sister to sequences from the angiosperm taxa, which formed a strongly supported (100% bootstrap, 1.00 Bayesian) clade. These results all reflect previously reported Class III HD ZIP gene family relationships [17], [20]. Among the angiosperm sequences, three strongly supported clades were formed, REV, PHB/PHV, and C8, which is in agreement with previous reports [17]. REV and PHB/PHV clades are sister to each other forming a larger clade that is sister to C8. Relationships within each of the three clades are generally consistent with currently accepted ideas about angiosperm phylogeny [34]. Our analysis includes four representative species from the grass lineage; O. sativus, Z. mays, B. distachyon, and S. bicolor, allowing further details in the divergence of homologues within this monocot lineage. Sequences from these four species form monophyletic clades separate from the eudicot species. Within these clades two duplication events appear to have occurred after the monocot-eudicot split. This duplication likely represents the grass whole genome duplication event [35], [36].


The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems.

Du J, Miura E, Robischon M, Martinez C, Groover A - PLoS ONE (2011)

Phylogenetic relationships among Class III HD ZIP gene family in land plants determined using maximum parsimony analysis.Bootstrap support values above 50% are presented above branches and Bayesian support values above 0.50 are presented below branches, where * indicates maximum 1.00 support. Black squares indicate major duplication events, while the empty square represents evidence of a duplication event without bootstrap support. Major clades are presented by longitudinal lines to the right of the tree, where solid lines represent fully supported monophyletic clades (PHB, C8, and CNA) and dashed lines indicate clade supported by Bayesian, but not bootstrap support. Black triangles represent where the AtHB8, AlHB8, MgHB7 clade is supported according to Bayesian analysis. Species abbreviations: At, Arabidopsis thaliana; Bd, Brachypodium distachyon; Al, Arabidopsis lyrata; Cp, Carica papaya; Cs, Cucumis sativus; Gm, Glycine max; Me, Manihot esculenta; Mt, Medicago truncatula; Mg, Mimulus guttatus; Os, Oryzas sativa; Pt, Populus trichocarpa; Pp, Physcomitrella patens; Rc, Ricinus communis; Sm, Selanginella moellendorffii, Sb, Sorghum bicolor; Vv, Vitis vinifera; Zm, Zea mays.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3046250&req=5

pone-0017458-g001: Phylogenetic relationships among Class III HD ZIP gene family in land plants determined using maximum parsimony analysis.Bootstrap support values above 50% are presented above branches and Bayesian support values above 0.50 are presented below branches, where * indicates maximum 1.00 support. Black squares indicate major duplication events, while the empty square represents evidence of a duplication event without bootstrap support. Major clades are presented by longitudinal lines to the right of the tree, where solid lines represent fully supported monophyletic clades (PHB, C8, and CNA) and dashed lines indicate clade supported by Bayesian, but not bootstrap support. Black triangles represent where the AtHB8, AlHB8, MgHB7 clade is supported according to Bayesian analysis. Species abbreviations: At, Arabidopsis thaliana; Bd, Brachypodium distachyon; Al, Arabidopsis lyrata; Cp, Carica papaya; Cs, Cucumis sativus; Gm, Glycine max; Me, Manihot esculenta; Mt, Medicago truncatula; Mg, Mimulus guttatus; Os, Oryzas sativa; Pt, Populus trichocarpa; Pp, Physcomitrella patens; Rc, Ricinus communis; Sm, Selanginella moellendorffii, Sb, Sorghum bicolor; Vv, Vitis vinifera; Zm, Zea mays.
Mentions: The POPCORONA (PCN) gene (also called Pt-ATHB.12; Joint Genome Institute Populus v.1.1 gene model fgenesh4_pm.C_LG_I000560; Phytozome Populus v2.0 gene model POPTR_0001s18930: GenBank XM_002299699) was amplified from cDNA of the sequenced Populus trichocarpa individual [33] based on similarity to the Arabidopsis thaliana ATHB15/CORONA (Materials and Methods). To determine the relationship of PCN to other Class III HD ZIPs, a phylogenetic analysis of Class III HD ZIP sequences from whole-genome sequencing projects was undertaken (Materials and Methods). Maximum parsimony analysis from the nucleotide sequence alignment of the coding sequences of Class III HD ZIPs found in 17 plant species and deduced from amino acid sequence alignments yielded a single tree, with clade support from Bayesian and bootstrap analysis (Fig. 1). Sequences from Physcomitrella patens, a moss, were used as outgroups to root the tree. Sequences from the lycophyte representative, Selanginella moellendorffii, formed a clade (53% bootstrap, 1.00 Bayesian) sister to sequences from the angiosperm taxa, which formed a strongly supported (100% bootstrap, 1.00 Bayesian) clade. These results all reflect previously reported Class III HD ZIP gene family relationships [17], [20]. Among the angiosperm sequences, three strongly supported clades were formed, REV, PHB/PHV, and C8, which is in agreement with previous reports [17]. REV and PHB/PHV clades are sister to each other forming a larger clade that is sister to C8. Relationships within each of the three clades are generally consistent with currently accepted ideas about angiosperm phylogeny [34]. Our analysis includes four representative species from the grass lineage; O. sativus, Z. mays, B. distachyon, and S. bicolor, allowing further details in the divergence of homologues within this monocot lineage. Sequences from these four species form monophyletic clades separate from the eudicot species. Within these clades two duplication events appear to have occurred after the monocot-eudicot split. This duplication likely represents the grass whole genome duplication event [35], [36].

Bottom Line: Synthetic miRNA knock down of POPCORONA results in abnormal lignification in cells of the pith, while overexpression of a miRNA-resistant POPCORONA results in delayed lignification of xylem and phloem fibers during secondary growth.POPCORONA misexpression also results in coordinated changes in expression of genes within a previously described transcriptional network regulating cell differentiation and cell wall biosynthesis, and hormone-related genes associated with fiber differentiation.POPCORONA illustrates another function of Class III HD ZIPs: regulating cell differentiation during secondary growth.

View Article: PubMed Central - PubMed

Affiliation: Institute of Forest Genetics, Pacific Southwest Research Station, U.S. Forest Service, Davis, California, United States of America.

ABSTRACT
The developmental mechanisms regulating cell differentiation and patterning during the secondary growth of woody tissues are poorly understood. Class III HD ZIP transcription factors are evolutionarily ancient and play fundamental roles in various aspects of plant development. Here we investigate the role of a Class III HD ZIP transcription factor, POPCORONA, during secondary growth of woody stems. Transgenic Populus (poplar) trees expressing either a miRNA-resistant POPCORONA or a synthetic miRNA targeting POPCORONA were used to infer function of POPCORONA during secondary growth. Whole plant, histological, and gene expression changes were compared for transgenic and wild-type control plants. Synthetic miRNA knock down of POPCORONA results in abnormal lignification in cells of the pith, while overexpression of a miRNA-resistant POPCORONA results in delayed lignification of xylem and phloem fibers during secondary growth. POPCORONA misexpression also results in coordinated changes in expression of genes within a previously described transcriptional network regulating cell differentiation and cell wall biosynthesis, and hormone-related genes associated with fiber differentiation. POPCORONA illustrates another function of Class III HD ZIPs: regulating cell differentiation during secondary growth.

Show MeSH