Functional network analysis of genes differentially expressed during xylogenesis insoc1fulwoody Arabidopsis plants

Abstract

SUMMARYMany plant genes are known to be involved in the development of cambium and wood, but how the expression and functional interaction of these genes determine the unique biology of wood remains largely unknown. We used the soc1ful loss of function mutant -the woodiest genotype known in the otherwise herbaceous model plant Arabidopsis -to investigate the expression and interactions of genes involved in secondary growth (wood formation). Detailed anatomical observations of the stem in combination with mRNA sequencing were used to assess transcriptome remodeling during xylogenesis in wild-type and woody soc1ful plants. To interpret the transcriptome changes, we constructed functional gene association networks of differentially expressed genes using the STRING database. This analysis revealed functionally enriched gene association hubs that are differentially expressed in herbaceous and woody tissues. In particular, we observed the differential expression of genes related to mechanical stress and jasmonate biosynthesis/signaling during wood formation in soc1ful plants that may be an effect of greater tension within woody tissues. Our results suggest that habit shifts from herbaceous to woody life forms observed in many angiosperm lineages could have evolved convergently by genetic changes that modulate the gene expression and interaction network, and thereby redeploy the conserved wood developmental program.

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

“…To date, molecular understanding regarding how the ring of vascular cambium is developed in woody species is limited due to challenges faced in performing forward genetic analysis in trees. The herbaceous species Arabidopsis has been used in several studies as a research model to screen for mutants or to induce secondary growth with hormone treatment (Chaffey et al, 2002;Davin et al, 2016;Ko et al, 2004;Zhang et al, 2011). A number of genes has been identified for their role in regulating Arabidopsis cambium activity Parker et al, 2003;Pineau et al, 2005;Suer et al, 2011).…”

Parallel evolution of arborescent carrots (Daucus) in Macaronesia

“…Experimental data on the model plant Arabidopsis thaliana suggest that the gain of a prominent wood cylinder requires small genetic changes (Chaffey et al, 2002;Ko et al, 2004;Melzer et al, 2008;Lens et al, 2012b;Rowe and Paul-Victor, 2012;Davin et al, 2016); therefore, derived woodiness may evolve in a relatively short time. However, even though derived woodiness is a widespread phenomenon found in many families (Park et al, 2001;Barber et al, 2002;Francisco-Ortega et al, 2002;Lee et al, 2005;Nürk et al, 2019), the ages of derived and, in particular, insular woody clades remain mostly unknown (Kim et al, 2008), obstructing our understanding of the possible causes and mechanisms leading to the evolution of derived woodiness.…”

Co-expression network of secondary cell wall biogenesis genes in Eucalyptus tereticornis

“…The recent approach of systems genetics has enabled a deeper understanding on secondary development with an insight into the critically essential genes, pathways and networks which are unique to wood formation in tree species (Mizrachi and Myburg, 2016;Mizrachi et al, 2017). Gene networks for secondary cell wall formation are reported in several species like Arabidopsis (Yang et al, 2011;Ruprecht and Persson, 2012;Taylor-Teeples et al, 2015;Davin et al, 2016), poplars (Yang et al, 2011;Cai et al, 2014;Liu et al, 2015;Lamara et al, 2016;Zinkgraf et al, 2017;Shi et al, 2017), Pinus taeda (Palle et al, 2011), sugarcane (Ferreira et al, 2016), rice (Guo et al, 2014;Chandran et al, 2016). Recently, in E. grandis × E. urophylla hybrid population, a network based eQTL analysis tagging biomass and bio-energy related traits was reported.…”

“…Hence, with the introduction of high throughput genomics technologies along with comprehensive computational pipelines, a holistic systems genetics perspective to comprehend the molecular architecture of complex trait like wood formation has emerged. Presently, genome-scale analyses of SCW biogenesis are reported and gene regulatory networks specific to SCW formation is documented in Arabidopsis, poplar, pine, spruce, rice and sugarcane (Yang et al, 2011;Palle et al, 2011;Ruprecht and Persson, 2012;Vanholme et al, 2012;Hirano et al, 2013;Cai et al, 2014;Taylor-Teeples et al, 2015;Lamara et al, 2016;Liu et al, 2015;Chandran et al, 2016;Davin et al, 2016;Ferreira et al, 2016;Zinkgraf et al, 2017;Shi et al, 2017;Jokipii-Lukkari et al, 2018).…”