Coordinated Genetic Regulation of Growth and Lignin Revealed by Quantitative Trait Locus Analysis of cDNA Microarray Data in an Interspecific Backcross of Eucalyptus

Abstract

Phenotypic, genotypic, and transcript level (microarray) data from an interspecific backcross population of Eucalyptus grandis and Eucalyptus globulus were integrated to dissect the genetic and metabolic network underlying growth variation. Transcript abundance, measured for 2,608 genes in the differentiating xylem of a 91 (E. grandis 3 E. globulus) 3 E. grandis backcross progeny was correlated with diameter variation, revealing coordinated down-regulation of genes encoding enzymes of the lignin biosynthesis and associated methylation pathways in fast growing individuals. Lignin analysis of wood samples confirmed the content and quality predicted by the transcript levels measured on the microarrays. Quantitative trait locus (QTL) analysis of transcript levels of lignin-related genes showed that their mRNA abundance is regulated by two genetic loci, demonstrating coordinated genetic control over lignin biosynthesis. These two loci colocalize with QTLs for growth, suggesting that the same genomic regions are regulating growth, and lignin content and composition in the progeny. Genetic mapping of the lignin genes revealed that most of the key biosynthetic genes do not colocalize with growth and transcript level QTLs, with the exception of the locus encoding the enzyme S-adenosylmethionine synthase. This study illustrates the power of integrating quantitative analysis of gene expression data and genetic map information to discover genetic and metabolic networks regulating complex biological traits.Wood is composed of secondary xylem, a highly specialized conductive and structural support tissue produced by lateral growth and differentiation of the meristematic vascular cambium (Fukuda, 1996). Genes expressed during the developmentally regulated process of xylogenesis determine the physical and chemical properties of wood. The product of xylogenesis represents one of the world's most important natural resources, yet relatively little is known about the genetic regulation of this process. Wood serves as a renewable source of energy, and it is a sink for atmospheric carbon. Wood is also the raw material for the global pulp and paper, and timber industries. The growth and development of trees and other woody plants are fundamental determinants of the dynamics and composition of forest ecosystems.At the plant cell level, growth is determined by cell division and expansion. Expansion is driven primarily by internal osmotic pressure generated by water uptake. Expansion is constrained by the cell wall and depends on cell wall composition and the degree of association between its different components (Buchanan et al., 2000). Growth of secondary xylem results from a sequential developmental process that begins with cambial cell division, followed by cell expansion, secondary wall formation, lignification, and programmed cell death (Fukuda, 1996). Wood growth has been associated with the number and rate of cell divisions at the meristematic cambium (Gregory and Wilson, 1968;Wilson and Howard, 1968;Zobel and van Buijtenen, 1989...

Lignin and Biomass: A Negative Correlation for Wood Formation and Lignin Content in Trees

“…Similar to the results previously observed in Eucalyptus (Kirst et al, 2004), expression of lignin biosynthesis genes was coordinated with aboveground growth in the segregating family of Populus analyzed by Novaes et al (2009). Analysis of this population with whole-transcriptome microarrays developed to discriminate among members of gene families ( Fig.…”

“…1A; Kirst et al, 2004). Chemical analysis of wood from individual trees demonstrated a 10% reduction in lignin among the fastest-growing trees relative to slow growers and an increase in the S/G ratio in slow-growing trees (Kirst et al, 2004).…”

“…growth) but also occurs in response to environmental cues, such as nitrogen, Suc, and Phe availability (Anterola et al, 2002;Kirst et al, 2004;Scheible et al, 2004). This coordinated transcription extends beyond the phenylpropanoid pathway, including genes in the biosynthesis of aromatic amino acid precursors for Phe and S-adenosylmethionine (Anterola et al, 2002;Kirst et al, 2004). Quantitative trait locus (QTL) mapping of phenotypes and expression QTL mapping of transcript level variation provides locations of genomic regions containing candidate genes responsible for coordinate control.…”

“…Studies in populations of forest tree hybrids have shown a negative correlation of biomass growth (usually measured as wood volume) and lignin content (Kirst et al, 2004;Novaes et al, 2009). The control of growth and lignin appears to be highly regulated, implying that selection for improved growth rate could effect a reduction in lignin content.…”

Fine mapping of regulatory loci for mammalian gene expression using radiation hybrids

“…To date, expression quantitative trait loci, or eQTLs, have been mapped in populations segregating polymorphisms [2][3][4][5][6][7][8][9][10][11][12] , but power in such studies is limited by the frequency of ~1 crossover per chromosome per meiosis.…”