Wood Formation in Trees Is Increased by Manipulating PXY-Regulated Cell Division

Abstract

The woody tissue of trees is composed of xylem cells that arise from divisions of stem cells within the cambial meristem. The rate of xylem cell formation is dependent upon the rate of cell division within the cambium and is controlled by both genetic and environmental factors [1Miyashima S. Sebastian J. Lee J.Y. Helariutta Y. Stem cell function during plant vascular development.EMBO J. 2013; 32: 178-193Crossref PubMed Scopus (155) Google Scholar, 2Ursache R. Nieminen K. Helariutta Y. Genetic and hormonal regulation of cambial development.Physiol. Plant. 2013; 147: 36-45Crossref PubMed Scopus (56) Google Scholar]. In the annual plant Arabidopsis, signaling between a peptide ligand CLE41 and a receptor kinase PXY controls cambial cell divisions [3Etchells J.P. Turner S.R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division.Development. 2010; 137: 767-774Crossref PubMed Scopus (245) Google Scholar, 4Fisher K. Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development.Curr. Biol. 2007; 17: 1061-1066Abstract Full Text Full Text PDF PubMed Scopus (285) Google Scholar, 5Hirakawa Y. Shinohara H. Kondo Y. Inoue A. Nakanomyo I. Ogawa M. Sawa S. Ohashi-Ito K. Matsubayashi Y. Fukuda H. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system.Proc. Natl. Acad. Sci. USA. 2008; 105: 15208-15213Crossref PubMed Scopus (379) Google Scholar]; however, the pathway regulating secondary growth in trees has not been identified. Here, we show that an aspen receptor kinase PttPXY and its peptide ligand PttCLE41 are functional orthologs and act to control a multifunctional pathway that regulates both the rate of cambial cell division and woody tissue organization. Ectopic overexpression of PttPXY and PttCLE41 genes in hybrid aspen resulted in vascular tissue abnormalities and poor plant growth. In contrast, precise tissue-specific overexpression generated trees that exhibited a 2-fold increase in the rate of wood formation, were taller, and possessed larger leaves compared to the controls. Our results demonstrate that the PXY-CLE pathway has evolved to regulate secondary growth and manipulating this pathway can result in dramatically increased tree growth and productivity.