Transcription Reprogramming during Root Nodule Development in Medicago truncatula

Abstract

Many genes which are associated with root nodule development and activity in the model legume Medicago truncatula have been described. However information on precise stages of activation of these genes and their corresponding transcriptional regulators is often lacking. Whether these regulators are shared with other plant developmental programs also remains an open question. Here detailed microarray analyses have been used to study the transcriptome of root nodules induced by either wild type or mutant strains of Sinorhizobium meliloti. In this way we have defined eight major activation patterns in nodules and identified associated potential regulatory genes. We have shown that transcription reprogramming during consecutive stages of nodule differentiation occurs in four major phases, respectively associated with (i) early signalling events and/or bacterial infection; plant cell differentiation that is either (ii) independent or (iii) dependent on bacteroid differentiation; (iv) nitrogen fixation. Differential expression of several genes involved in cytokinin biosynthesis was observed in early symbiotic nodule zones, suggesting that cytokinin levels are actively controlled in this region. Taking advantage of databases recently developed for M. truncatula, we identified a small subset of gene expression regulators that were exclusively or predominantly expressed in nodules, whereas most other regulators were also activated under other conditions, and notably in response to abiotic or biotic stresses. We found evidence suggesting the activation of the jasmonate pathway in both wild type and mutant nodules, thus raising questions about the role of jasmonate during nodule development. Finally, quantitative RT-PCR was used to analyse the expression of a series of nodule regulator and marker genes at early symbiotic stages in roots and allowed us to distinguish several early stages of gene expression activation or repression.

Changes in the Common Bean Transcriptome in Response to Secreted and Surface Signal Molecules of Rhizobium etli

“…Other transcription factors represented in our list include MYB transcription factors, which participate in metabolism, response to stress, and synthesis of the cell wall (Dubos et al, 2010;Ko et al, 2014), as well as other families implicated in several aspects of plant development and stress responses. Similar results were reported in nodules of M. truncatula, where MYB, Homeobox (HB), RWP-RK, basic Leucine Zipper (bZIP), basic HelixLoop-Helix (bHLH), Cys2-His2 (C2H2), NAC, Zinc finger, Zinc-finger protein expressed in Inflorescence Meristem (ZIM) domain, ERF, and GRAS transcription factors were differentially expressed in nodules or in infected root hairs (Moreau et al, 2011;Breakspear et al, 2014).…”

Expression Dynamics of the Medicago truncatula Transcriptome during the Symbiotic Interaction with Sinorhizobium meliloti: Which Role for Nitric Oxide?

“…Over the past 10 years, hundreds of plant and bacterial genes displaying differential expression during the nodulation process have been identified by transcriptome analyses in M. truncatula and S. meliloti El Yahyaoui et al, 2004;Capela et al, 2006;Starker et al, 2006;Benedito et al, 2008;Jones et al, 2008;Maunoury et al, 2010;Moreau et al, 2011). Studies of bacterial and plant mutants have led to the identification of plant genes involved in early stages of the symbiotic interaction (Mitra and Long, 2004).…”

“…This study demonstrated that a two-stage reprogramming of gene expression takes place during nodule formation. More recently, more than 3,400 differentially regulated genes and associated regulators have been identified in studies with a 16.4 K 70-mer oligonucleotide microarray (Moreau et al, 2011); this analysis led to the definition of four different stages of transcription reprogramming during the course of nodulation. Additional resources relevant to M. truncatula functional genomics include the M. truncatula Gene Expression Atlas (http:// mtgea.noble.org/v3/), which provides developmental expression data for most of the genes of M. truncatula (Benedito et al, 2008).…”

How legumes recognize rhizobia

“…Some of these genes seems to be involved in meristem activity and differentiation, including genes that participate in cytokinin synthesis and activation. 30 At 10 days after inoculation, a group of plant defense genes showed higher mRNA levels in plants inoculated with exoA, although they were still expressed in response to the wild type strain of S. meliloti, providing partial support to the proposed role of EPS in the limitation of plant defense responses.…”

“…Of particular interest are studies that used mutant strains of rhizobia to dissect the transcriptional changes associated to recognition of signal molecules from bacteria. 28,[30][31][32][33] (Table 1). Jones and collaborators 32 showed the differences in the M. truncatula transcriptional response when it was inoculated with the wild type strain or a succinoglycan-deficient strain of S. meliloti unable to establish a successful infection.…”