A HD‐ZIP III gene, PtrHB4, is required for interfascicular cambium development in Populus

Zhu, Yingying; Song, Dongli; Xu, Peng; Sun, Jing; Li, Laigeng

doi:10.1111/pbi.12830

Cited by 59 publications

(70 citation statements)

References 47 publications

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“…The WUSCHEL-RELATED HOMEOBOX gene WOX4 is a downstream target of PXY and is essential for promoting cambial cell division in stems (Suer et al, 2011;Etchells et al, 2013). The Populus HD-ZIP III gene family members PtrHB2 and PtrHB4 play key roles in the regulation of cell division in the procambium/cambium (Robischon et al, 2011;Zhu et al, 2018). However, this ERF pathway is repressed by PXY signaling (Etchells et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Dual regulation of xylem formation by an auxin‐mediated PaC3H17‐PaMYB199 module in Populus

et al. 2019

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Summary Wood (secondary xylem) formation in tree species is dependent on auxin‐mediated vascular cambium activity in stems. However, the complex regulatory networks underlying xylem formation remain elusive. Xylem development in Populus was characterized based on microscopic observations of stem sections in transgenic plants. Transcriptomic, quantitative real‐time PCR, chromatin immunoprecipitation PCR, and electrophoretic mobility shift assay analyses were conducted to identify target genes involved in xylem development. Yeast two‐hybrid, pull‐down, bimolecular fluorescence complementation, and co‐immunoprecipitation assays were used to validate protein–protein interactions. PaC3H17 and its target PaMYB199 were found to be predominantly expressed in the vascular cambium and developing secondary xylem in Populus stems and play opposite roles in controlling cambial cell proliferation and secondary cell wall thickening through an overlapping pathway. Further, PaC3H17 interacts with PaMYB199 to form a complex, attenuating PaMYB199‐driven suppression of its xylem targets. Exogenous auxin application enhances the dual control of the PaC3H17‐PaMYB199 module during cambium division, thereby promoting secondary cell wall deposition. Dual regulation of xylem formation by an auxin‐mediated PaC3H17‐PaMYB199 module represents a novel regulatory mechanism in Populus, increasing our understanding of the regulatory networks involved in wood formation.

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Section: Introductionmentioning

confidence: 99%

Dual regulation of xylem formation by an auxin‐mediated PaC3H17‐PaMYB199 module in Populus

et al. 2019

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“…5c). The expression levels of the class III homeodomain-leucine zipper (HD-Zip III) transcription factor genes PttHB4 (Zhu et al, 2018) and PttHB7 (Zhu et al, 2013) was dramatically reduced in the stems of RNAi lines, both with respect to similar age and developmental stage of WT stems (Fig. 5c).…”

Section: Researchmentioning

confidence: 99%

“…In Arabidopsis, HD-Zip IIIs have recently been shown to position and maintain cambial stem cells (Smetana et al, 2019). In poplar, HD-Zip III transcription factors are required for cambium development (Robischon et al, 2011;Zhu et al, 2013Zhu et al, , 2018. In particular, PtrHB4 is critical for the formation of a closed vascular cambium ring from fascicular and interfascicular cambium (Zhu et al, 2018).…”

Section: Researchmentioning

confidence: 99%

Peptide encoding Populus CLV3/ESR‐RELATED 47 (PttCLE47) promotes cambial development and secondary xylem formation in hybrid aspen

et al. 2019

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Summary The CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION (ESR)‐RELATED (CLE) peptide ligands in connection with their receptors are important players in cell‐to‐cell communications in plants. Here, we investigated the function of the Populus CLV3/ESR‐RELATED 47 (PttCLE47) gene during secondary growth and wood formation in hybrid aspen (Populus tremula × tremuloides) using an RNA interference (RNAi) approach. Expression of PttCLE47 peaks in the vascular cambium. Silencing of the PttCLE47 gene expression affected lateral expansion of stems and decreased apical height growth and leaf size. In particular, PttCLE47 RNAi trees exhibited a narrower secondary xylem zone with less xylem cells/cell file. The reduced radial growth phenotype also correlated with a reduced number of cambial cell layers. In agreement with these results, expression of several cambial regulator genes was downregulated in the stems of the transgenic trees in comparison with controls. Altogether, these results suggest that the PttCLE47 gene is a major positive regulator of cambial activity in hybrid aspen, mainly promoting the production of secondary xylem. Furthermore, in contrast to previously characterized CLE genes expressed in the wood‐forming zone, PttCLE47 appears to be active at its site of expression.

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“…Although primary and secondary vascular tissues in seed plants are derived from different meristematic cell populations, both are produced by precise patterning of the same suite of cell types. Accordingly, some of the same gene families or genetic modules function in both developmental contexts (7,9,11,12): the CLAVATA (CLE)-WUSCHEL (WOX) regulatory loop promotes meristem identity at the cost of xylem formation (13)(14)(15)(16), while multiple HD-ZIP III family members promote xylem differentiation and bipolar patterning of daughter cell types (17)(18)(19)(20)(21) [SI Appendix, Figure S1]. The functions of HD-ZIP III members and CLE-WOX modules have been documented during primary and secondary vascular differentiation in distantly related eudicots, including Arabidopsis thaliana, Populus trichocarpa, and Zinnia elegans, using loss-of-function and/or over-expression studies (8,9,22,23).…”

Section: Introductionmentioning

confidence: 99%

Water lily (Nymphaea thermarum) draft genome reveals variable genomic signatures of ancient vascular cambium losses

Povilus

DaCosta

Grassa

et al. 2019

Preprint

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For more than 225 million years, all seed plants were woody trees, shrubs, or vines (1)(2)(3)(4). Shortly after the origin of angiosperms ~135 million years ago (MYA) (5), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium (6), the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem (7-9), which are produced by apical meristems and retained in nearly all seed plants. Here we sequence and assemble a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compare it to genomes from other cambium-bearing and cambium-less lineages (like monocots and Nelumbo). This reveals lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also find the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent vascular cambium loss reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent trait loss events. Our results shed light on the evolution of herbaceousness -one of the key biological innovations associated with the earliest phases of angiosperm evolution.

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A HD‐ZIP III gene, PtrHB4, is required for interfascicular cambium development in Populus

Cited by 59 publications

References 47 publications

Dual regulation of xylem formation by an auxin‐mediated PaC3H17‐PaMYB199 module in Populus

Dual regulation of xylem formation by an auxin‐mediated PaC3H17‐PaMYB199 module in Populus

Peptide encoding Populus CLV3/ESR‐RELATED 47 (PttCLE47) promotes cambial development and secondary xylem formation in hybrid aspen

Water lily (Nymphaea thermarum) draft genome reveals variable genomic signatures of ancient vascular cambium losses

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