Symbiosis and the social network of higher plants

Venkateshwaran, Muthusubramanian; Volkening, Jeremy D.; Sussman, Michael R.; Ané, Jean‐Michel

doi:10.1016/j.pbi.2012.11.007

Cited by 122 publications

(111 citation statements)

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“…Over the past decade, researchers have elucidated a Nod factor perception and signaling pathway in legumes and an overlapping mycorrhizal pathway in both legumes and nonlegumes (for review, see Venkateshwaran et al, 2013). Nod factor receptors, which include Lysine motif domain-containing receptorlike kinase3 (LYK3) and Nodulation factor perception (NFP) in Medicago truncatula and Nodulation factor receptor1 (NFR1) and NFR5 in Lotus japonicus, are plasma membrane-localized receptor-like kinase and kinase-like (RLK) proteins (Amor et al, 2003;Smit et al, 2007;Haney et al, 2011;Moling et al, 2014) consisting of an intracellular kinase domain and an extracellular region with two or three chitin-binding Lys motifs (LysM).…”

mentioning

confidence: 99%

“…DMI3 (CCaMK in L. japonicus), a calcium and calmodulindependent protein kinase, presumably decodes the nuclear calcium oscillations and activates a transcriptional cascade Mitra et al, 2004;Singh and Parniske, 2012). A diverse suite of symbiotic transcription factors (TFs), including the GRAS family proteins NODULATION-SIGNALING PATHWAY1 (NSP1) and NSP2, the NODULE INCEPTION1 protein, NUCLEAR FACTOR-Y A1 and B1 (NF-YA1 and NF-YB1), and several members of the APETALA2 (AP2)/ETHYLENE RESPONSE FACTOR (ERF) family of TFs, mediate symbiotic gene expression and are each essential for symbiotic infection and nodule organogenesis (Oldroyd et al, 2011;Venkateshwaran et al, 2013).…”

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confidence: 99%

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Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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The legume-rhizobium symbiosis is initiated through the activation of the Nodulation (Nod) factor-signaling cascade, leading to a rapid reprogramming of host cell developmental pathways. In this work, we combine transcriptome sequencing with molecular genetics and network analysis to quantify and categorize the transcriptional changes occurring in roots of Medicago truncatula from minutes to days after inoculation with Sinorhizobium medicae. To identify the nature of the inductive and regulatory cues, we employed mutants with absent or decreased Nod factor sensitivities (i.e. Nodulation factor perception and Lysine motif domain-containing receptor-like kinase3, respectively) and an ethylene (ET)-insensitive, Nod factor-hypersensitive mutant (sickle). This unique data set encompasses nine time points, allowing observation of the symbiotic regulation of diverse biological processes with high temporal resolution. Among the many outputs of the study is the early Nod factorinduced, ET-regulated expression of ET signaling and biosynthesis genes. Coupled with the observation of massive transcriptional derepression in the ET-insensitive background, these results suggest that Nod factor signaling activates ET production to attenuate its own signal. Promoter:b-glucuronidase fusions report ET biosynthesis both in root hairs responding to rhizobium as well as in meristematic tissue during nodule organogenesis and growth, indicating that ET signaling functions at multiple developmental stages during symbiosis. In addition, we identified thousands of novel candidate genes undergoing Nod factor-dependent, ET-regulated expression. We leveraged the power of this large data set to model Nod factor-and ET-regulated signaling networks using MERLIN, a regulatory network inference algorithm. These analyses predict key nodes regulating the biological process impacted by Nod factor perception. We have made these results available to the research community through a searchable online resource.

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confidence: 99%

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confidence: 99%

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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“…These two types of endosymbiotic associations require a common set of genes in host plants to allow successful bacterial and fungal colonization. The molecular mechanisms controlling the establishment of the legume-rhizobium symbiosis have been extensively studied in model legumes such as Medicago truncatula and Lotus japonicus (2,3). Rhizobia secrete lipochitooligosaccharides (LCOs) known as nodulation (Nod) factors, which are perceived by LysMtype receptor kinases, such as Nod factor perception (NFP) and LYK3 in M. truncatula and are required for both rhizobial infection and nodule organogenesis (4,5).…”

mentioning

confidence: 99%

A role for the mevalonate pathway in early plant symbiotic signaling

Venkateshwaran

Jayaraman

Chabaud

et al. 2015

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

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117

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Rhizobia and arbuscular mycorrhizal fungi produce signals that are perceived by host legume receptors at the plasma membrane and trigger sustained oscillations of the nuclear and perinuclear Ca2+ concentration (Ca2+ spiking), which in turn leads to gene expression and downstream symbiotic responses. The activation of Ca2+ spiking requires the plasma membrane-localized receptor-like kinase Does not Make Infections 2 (DMI2) as well as the nuclear cation channel DMI1. A key enzyme regulating the mevalonate (MVA) pathway, 3-Hydroxy-3-Methylglutaryl CoA Reductase 1 (HMGR1), interacts with DMI2 and is required for the legume–rhizobium symbiosis. Here, we show that HMGR1 is required to initiate Ca2+ spiking and symbiotic gene expression in Medicago truncatula roots in response to rhizobial and arbuscular mycorrhizal fungal signals. Furthermore, MVA, the direct product of HMGR1 activity, is sufficient to induce nuclear-associated Ca2+ spiking and symbiotic gene expression in both wild-type plants and dmi2 mutants, but interestingly not in dmi1 mutants. Finally, MVA induced Ca2+ spiking in Human Embryonic Kidney 293 cells expressing DMI1. This demonstrates that the nuclear cation channel DMI1 is sufficient to support MVA-induced Ca2+ spiking in this heterologous system.

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“…The discovery of a "common symbiotic pathway" in arbuscular mycorrhizal, rhizobial, and actinorhizal symbioses and the identification of conserved pathway genes (CSSP or SYM pathway) in legumes and monocots (including rice) has made the extension of the ability to fix nitrogen in nodular associations with cereals a more realistic endeavour [8] [9].…”

Section: The Common Symbiotic Signalling Pathway (Cssp or Sym)mentioning

confidence: 99%

“Biological Nitrogen Fixation” Book Summary

Bruijn¹

2016

AiM

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Biological nitrogen fixation is a very valuable alternative to nitrogen fertilizer. This process will be discussed in the "Biological Nitrogen Fixation" book. A wide array of free-living and associative nitrogen fixing organisms (diazotrophs) will be covered. The most extensively studied and applied example of biological nitrogen fixation is the symbiotic interaction between nitrogen fixing "rhizobia" and legume plants. While legumes are important as major food and feed crops, cereals such as wheat, maize and rice are the primary food crops, but do not have this symbiotic nitrogen fixing interaction with rhizobia. It has thus been a "holy grail" to transfer the ability to fix nitrogen to the cereals and this topic will be also addressed in these books.

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Symbiosis and the social network of higher plants

Cited by 122 publications

References 112 publications

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

A role for the mevalonate pathway in early plant symbiotic signaling

“Biological Nitrogen Fixation” Book Summary

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