Biosynthesis of cellulose‐enriched tension wood in <i>Populus</i>: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis

Andersson‐Gunnerås, Sara; Mellerowicz, Ewa J.; Love, Jonathan; Segerman, Bo; Ohmiya, Yasunori; Coutinho, Pedro M.; Nilsson, Peter; Henrissat, Bernard; Moritz, Thomas; Sundberg, Björn

doi:10.1111/j.1365-313x.2005.02584.x

Cited by 350 publications

(318 citation statements)

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“…In fact the plastidial pyruvate kinase has been involved in fatty acid synthesis in Arabidopsis seeds (Andre et al 2007;Baud et al 2007) and sucrose synthase is involved in oil accumulation, suggesting a coordination between glycolytic and fatty acid biosynthetic pathways (Troncoso-Ponce et al 2011). However, the upregulation of sucrose synthases in cork could also be a consequence of a higher demand of cell wall synthesis (Andersson-Gunnerås et al 2006;Wei et al 2015). In addition, we found several contigs showing significant homology with HXXXDmotif/BAHD acyltransferases and GDSL-like genes that are upregulated in cork oak outer bark (Table S6A) and although their role in the biosynthesis of suberin has not yet been described, they could also be relevant for the accumulation of this polyester according to the role of some members of these gene families (Girard et al 2012;Molina and Kosma 2015).…”

Section: Discussionmentioning

confidence: 99%

A comparative transcriptomic approach to understanding the formation of cork

et al. 2017

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Key message The transcriptome comparison of two oak species reveals possible candidates accounting for the exceptionally thick and pure cork oak phellem, such as those involved in secondary metabolism and phellogen activity. Abstract Cork oak, Quercus suber, differs from other Mediterranean oaks such as holm oak (Quercus ilex) by the thickness and organization of the external bark. While holm oak outer bark contains sequential periderms interspersed with dead secondary phloem (rhytidome), the cork oak outer bark only contains thick layers of phellem (cork rings) that accumulate until reaching a thickness that allows industrial uses. Here we compare the cork oak outer bark transcriptome with that of holm oak. Both transcriptomes present similitudes in their complexity, but whereas cork oak external bark is enriched with upregulated genes related to suberin, which is the main polymer responsible for the protective function of periderm, the upregulated categories of holm oak are enriched in abiotic stress and chromatin assembly. Concomitantly with the upregulation of suberin-related genes, there is also induction of regulatory and meristematic genes, whose predicted activities agree with the increased number of phellem layers found in the cork oak sample. Further transcript profiling among different cork oak tissues and conditions suggests that cork and wood share many regulatory mechanisms, probably reflecting similar ontogeny. Moreover, the analysis of transcripts accumulation during the cork growth season showed that most regulatory genes are upregulated early in the season when the cork cambium becomes active. Altogether our work provides the first transcriptome comparison between cork oak and holm oak outer bark, which unveils new regulatory candidate genes of phellem development.

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Section: Discussionmentioning

confidence: 99%

A comparative transcriptomic approach to understanding the formation of cork

et al. 2017

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“…It has been suggested that the prevalence of neutral PMEs in active cells would allow cell wall expansion (Guglielmino et al 1996). Pectinesterase transcripts were among the differentially regulated and most strongly expressed genes in tension wood of Populus (Andersson-Gunneras et al 2006) and in the juvenile cambial region of E. grandis (Gallo De Carvalho et al 2008). A pectin methyl esterase from wood-forming tissues of hybrid aspen (P. tremula x tremuloides Michx.)…”

Section: Resultsmentioning

confidence: 99%

Association Genetics of Wood Physical Traits in the Conifer White Spruce and Relationships With Gene Expression

et al. 2011

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Marker-assisted selection holds promise for highly influencing tree breeding, especially for wood traits, by considerably reducing breeding cycles and increasing selection accuracy. In this study, we used a candidate gene approach to test for associations between 944 single-nucleotide polymorphism markers from 549 candidate genes and 25 wood quality traits in white spruce. A mixed-linear model approach, including a weak but nonsignificant population structure, was implemented for each marker-trait combination. Relatedness among individuals was controlled using a kinship matrix estimated either from the known half-sib structure or from the markers. Both additive and dominance effect models were tested. Between 8 and 21 single-nucleotide polymorphisms (SNPs) were found to be significantly associated (P # 0.01) with each of earlywood, latewood, or total wood traits. After controlling for multiple testing (Q # 0.10), 13 SNPs were still significant across as many genes belonging to different families, each accounting for between 3 and 5% of the phenotypic variance in 10 wood characters. Transcript accumulation was determined for genes containing SNPs associated with these traits. Significantly different transcript levels (P # 0.05) were found among the SNP genotypes of a 1-aminocyclopropane-1-carboxylate oxidase, a b-tonoplast intrinsic protein, and a long-chain acyl-CoA synthetase 9. These results should contribute toward the development of efficient marker-assisted selection in an economically important tree species.

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“…TW is formed on the upper side of the leaning stem, resulting in characteristic asymmetric growth, and it serves to correct the stem position (4). In addition to the striking increase in cambial cell divisions, TW has an altered anatomy, and the fibers form an additional inner, cellulose-rich, gelatinous secondary cell wall layer (G layer) (5).…”

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Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus

Love

Björklund

Vahala

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The plant hormone ethylene is an important signal in plant growth responses to environmental cues. In vegetative growth, ethylene is generally considered as a regulator of cell expansion, but a role in the control of meristem growth has also been suggested based on pharmacological experiments and ethylene-overproducing mutants. In this study, we used transgenic ethylene-insensitive and ethylene-overproducing hybrid aspen (Populus tremula ؋ tremuloides) in combination with experiments using an ethylene perception inhibitor [1-methylcyclopropene (1-MCP)] to demonstrate that endogenous ethylene produced in response to leaning stimulates cell division in the cambial meristem. This ethylenecontrolled growth gives rise to the eccentricity of Populus stems that is formed in association with tension wood.plant hormones ͉ secondary xylem ͉ tension wood ͉ vascular cambium ͉ wood development T he vascular cambium is the meristem that produces secondary xylem and phloem by periclinal cell divisions, and it is responsible for wood production and stem diameter growth in trees. Cambial growth rate along the trunk is correlated with leaf biomass and crown structure (1). Superimposed on this intrinsic control, cambial growth is also strongly influenced by environment, where mechanical and gravitational loads imposed by wind and leaning are important (2). Wind sway induces increased diameter growth that protects against stem breakage (3), whereas a static lean results in a localized growth response known as tension wood (TW) in dicotyledonous angiosperms. TW is formed on the upper side of the leaning stem, resulting in characteristic asymmetric growth, and it serves to correct the stem position (4). In addition to the striking increase in cambial cell divisions, TW has an altered anatomy, and the fibers form an additional inner, cellulose-rich, gelatinous secondary cell wall layer (G layer) (5).Experiments with ethylene applications have revealed that this volatile plant hormone has the potential to both inhibit and stimulate growth (6). Its synthesis from S-adenosylmethionine through the action of 1-aminocyclopropane-1-carboxylate (ACC) synthase (ACS) and ACC oxidase (ACO) is triggered in vegetative tissues in response to many environmental cues. To date, concepts of ethylene function in vegetative growth have mainly implicated its role in primary tissue and cell expansion (6). However, ethylene biosynthesis increases during TW formation because of an asymmetric induction of ACO (7,8), and application of ethylene has been shown to stimulate cambial growth both in trees and herbaceous species (9, 10). Additional observations also support a potential role for ethylene in cell division. Applied ethylene stimulated endoreduplication in cucumber hypocotyls and growth of the intercalary meristem in deepwater rice (11-13). Moreover, the ethylene-overproducing Arabidopsis mutant eto1 exhibits aberrant cell divisions in the quiescent center of the root (14). However, experiments where ethylene homeostasis is artificially manipulated by a...

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Biosynthesis of cellulose‐enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis

Cited by 350 publications

References 80 publications

A comparative transcriptomic approach to understanding the formation of cork

A comparative transcriptomic approach to understanding the formation of cork

Association Genetics of Wood Physical Traits in the Conifer White Spruce and Relationships With Gene Expression

Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus

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