Gene Expression in Nitrogen-Fixing Symbiotic Nodule Cells in Medicago truncatula and Other Nodulating Plants

Abstract

Root nodules formed by plants of the nitrogen-fixing clade (NFC) are symbiotic organs that function in the maintenance and metabolic integration of large populations of nitrogen-fixing bacteria. These organs feature unique characteristics and processes, including their tissue organization, the presence of specific infection structures called infection threads, endocytotic uptake of bacteria, symbiotic cells carrying thousands of intracellular bacteria without signs of immune responses, and the integration of symbiont and host metabolism. The early stages of nodulation are governed by a few welldefined functions, which together constitute the common symbiosis-signaling pathway (CSSP). The CSSP activates a set of transcription factors (TFs) that orchestrate nodule organogenesis and infection. The later stages of nodule development require the activation of hundreds to thousands of genes, mostly expressed in symbiotic cells. Many of these genes are only active in symbiotic cells, reflecting the unique nature of nodules as plant structures. Although how the nodule-specific transcriptome is activated and connected to early CSSP-signaling is poorly understood, candidate TFs have been identified using transcriptomic approaches, and the importance of epigenetic and chromatin-based regulation has been demonstrated. We discuss how gene regulation analyses have advanced our understanding of nodule organogenesis, the functioning of symbiotic cells, and the evolution of symbiosis in the NFC.

Expression of N‐cycling genes of root microbiomes provides insights for sustaining oilseed crop production

“…Rather, relationships between gene abundances and biogeochemical processes need to be examined for each system before gene abundance can be used to infer a microbial biogeochemical process (Rocca et al ., 2015). On the other hand, a close relationship was confirmed between N 2 fixation activity and nifH gene expression but not with gene copy number (Tang et al ., 2017; Mergaert et al ., 2020). The abundance of nirS , nirK , nosZ , nxrA and amoA transcripts also correlated well with nitrogen transformation rates of nitrification and denitrification, and N‐cycling gene expression was affected by plant–soil microenvironment variation (He et al ., 2018; Brin et al ., 2019).…”

Parasponia: a missing piece of the evolutionary puzzle of nitrogen-fixing nodule symbiosis

“…Nevertheless, Mergaert et al suggests that an independent evolution of the trait cannot be excluded (Mergaert et al, 2019). Our comparative study on Parasponia and Trema may shed light on the likeliness of this viewpoint.…”

“…Comparative genomics studies to explain the current phylogeny distribution of nodulation (Mergaert et al, 2019). Together with gene functional analysis, one major finding from these studies is that the convergence of the common symbiosis signalling pathway (CSSP) exploited by the more ancient arbuscular mycorrhizal (AM) symbiosis (Gherbi et al, 2008;Markmann et al, 2008;Hocher et al, 2011;Tromas et al, 2012;Svistoonoff et al, 2013Svistoonoff et al, , 2014Granqvist et al, 2015;.…”

“…Markmann and Parniske 2009; Oldroyd and Dixon 2014; Stokstad 2016;Charpentier and Oldroyd 2010). Over the past two decades, crucial genes within the signal pathways underlying this symbiotic trait have been uncovered through studies in legumes and other nodulating plant species (Oldroyd 2013;Roy et al 2019;Mergaert et al 2019). The general consensus now is that the capacity to establish nitrogen-fixing root nodule symbiosis partially recruited from the symbiotic signalling pathway that is used by the more ancient arbuscular mycorrhiza (AM) symbiosis, which is widespread among higher plants(Oldroyd 2013; Oldroyd et al 2011;).…”

“…F-G, Diverged evolution of nitrogen-fixing symbiosis in Cycadophyta, Gunnera and Zygophyllaceae from NFC. Figure is modified based onMergaert et al (2019) with permission from the publisher.…”