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The Populus Homeobox Gene ARBORKNOX2 Regulates Secondary Growth in trees

ABSTRACT: Currently little is known about the genetic mechanisms regulating the vascular cambium or the secondary growth of stems. We show here that the Populus Class I KNOX homeobox gene ARBORKNOX2 (ARK2) regulates both cell division in the cambium region and the differentiation of daughter cells in secondary xylem and phloem. ARK2 is expressed in the shoot apical meristem, and the vascular cambium region, reflecting some overlap in the regulation of these meristems. ARK2 is expressed broadly in the cambium region and in differentiating lignified cells types before becoming progressively restricted to the cambium. Populus overexpressing ARK2 present stem phenotypes with precocious cambium formation, delayed differentiation of cambium daughter cells, a wider cambium region, and ultimately less phloem fibers and secondary xylem. In contrast, Populus expressing RNAi or amicroRNA that target ARK2 transcripts present precocious differentiation of secondary phloem fibers and xylem, and ultimately more secondary xylem tissue and thicker secondary cell walls in phloem fibers and secondary xylem cells. These phenotypes in turn correlate with changes in the expression of genes affecting cell division, auxin, and cell wall synthesis and lignification that indicate that ARK2 primarily affects woody tissue development by regulation of cell differentiation. Notably, wood properties associated with secondary cell wall synthesis are negatively associated with ARK2 expression, including lignin and cellulose content. Together, our results suggest that ARK2 functions primarily by negatively regulating cell differentiation during secondary growth. We propose that ARK2 may identify a co-evolved regulatory module that influences complex wood properties relevant to ecological, industrial, and biofuels applications.

ORGANISM(S): Populus sp. Populus

PROVIDER: GSE15595 | GEO | 2009/10/01

SECONDARY ACCESSION(S): PRJNA115607

REPOSITORIES: GEO

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Project description:Vascular cambium is a secondary meristem which produces xylem (wood) inwards and phloem (bark) outwards. The activity of cambium leads to expansion in the diameters in plants, that is, secondary growth, and thus contributes to biomass increase. The regulation of cambium development is at multilevel including phytohormones and peptide-receptor kinase (CLE41/44-PXY) signalling pathways. However, only limited progress has been made on the transcriptional regulation level. To construct the transcriptional network that regulates cambium development, we performed a genome wide transcript profiling in sorted procambial and cambial cells in Arabidopsis roots. More than 500 genes were identified as cambium abundant genes via comparison against transcriptomes of other Arabidopsis root cell types. We then investigated the roles of almost all the cambial transcription factors (TFs) and some of their homologous genes during secondary growth. Many of the candidate TFs were highly expressed in cambium based on the promoter GUS fusion and in situ hybridization. An unbiased transcriptional regulatory network was constructed using transcript profiling data collected from inducible overexpression lines for selected candidate TFs and a few major nodes were identified in the network including WOX4 and KNAT1. Moreover, the severity of mutant phenotypes was predicted based on the network. Next, we used the predication as a guide and generated over 70 double mutants within the same or among different TF families to explore the genetic interactions of candidate genes. Phenotype characterization on the secondary growth of the mutants and the overexpression lines identified promoters and inhibitors of cambium activity. The phenotypic data also suggested the redundancy within and among TF families because the phenotypes could be enhanced when additional TFs were mutated. We also found that combinations of certain overexpression lines and mutants led to pronounced increase of cell proliferation or xylem differentiation and in the extreme case the formation of ectopic cambium. We herein propose that cambium development is orchestrated by a wide network at the transcriptional level, where each TF has a different contribution to cell proliferation and differentiation.

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The Populus Homeobox Gene ARBORKNOX2 Regulates Secondary Growth in trees

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