NIN Acts as a Network Hub Controlling a Growth Module Required for Rhizobial Infection

Liu, Cheng-Wu; Breakspear, Andrew; Guan, Dian; Cerri, Marion R.; Jackson, Kirsty; Jiang, Suyu; Robson, Fran; Radhakrishnan, Guru V.; Roy, Sonali; Bone, Caitlin; Stacey, Nicola; Rogers, Christian; Trick, Martin; Niebel, Andréas; Oldroyd, Giles; Carvalho-Niebel, Fernanda de; Murray, Jeremy D.

doi:10.1104/pp.18.01572

Cited by 109 publications

(152 citation statements)

References 105 publications

(196 reference statements)

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“…NIN is the key regulator that coordinates rhizobial infection and nodule organogenesis (Vernié et al, 2015). NIN is required for the induction of many of the genes known to be associated with rhizobial infection in root hairs of M. truncatula (Liu et al, 2019). Several genes with NIN binding sites were identified previously (Soyano et al, 2014), and we confirmed NIN binds upstream of RINRK1.…”

Section: Discussionsupporting

confidence: 71%

“…Since the transcription factor NIN is associated with the regulation of several genes during rhizobial infection (Soyano et al, 2014;Liu et al, 2019), we tested whether RINRK1 was regulated by NIN. First, our RT-qPCR analysis revealed NF induction of RINRK1 was strongly reduced in the nin-2 mutant background ( Fig.…”

Section: Nin Directly Binds To the Rinrk1 Promoter And Induces Rinrk1mentioning

confidence: 99%

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Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus

Zheng

Kong

et al. 2019

Plant Physiol.

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During the legume-rhizobium symbiotic interaction, rhizobial invasion of legumes is primarily mediated by a plant-made tubular invagination called an infection thread (IT). Here, we identify a gene in Lotus japonicus encoding a Leu-rich repeat receptor-like kinase (LRR-RLK), RINRK1 (Rhizobial Infection Receptor-like Kinase1), that is induced by Nod factors (NFs) and is involved in IT formation but not nodule organogenesis. A paralog, RINRK2, plays a relatively minor role in infection. RINRK1 is required for full induction of early infection genes, including Nodule Inception (NIN), encoding an essential nodulation transcription factor. RINRK1 displayed an infection-specific expression pattern, and NIN bound to the RINRK1 promoter, inducing its expression. RINRK1 was found to be an atypical kinase localized to the plasma membrane and did not require kinase activity for rhizobial infection. We propose RINRK1 is an infection-specific RLK, which may specifically coordinate output from NF signaling or perceive an unknown signal required for rhizobial infection.

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Section: Discussionsupporting

confidence: 71%

Section: Nin Directly Binds To the Rinrk1 Promoter And Induces Rinrk1mentioning

confidence: 99%

Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus

Zheng

Kong

et al. 2019

Plant Physiol.

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“…Mtlyk10 mutants are thus symbiotic M. truncatula mutants that can uncouple infection and nodule organogenesis (Murray, ), revealing another plant component that is specifically involved in the infection process in M. truncatula . The expression profile of MtLYK10 is compatible with its role in infection, with strong induction in root hairs and nodules, and in response to either NFs or rhizobial inoculation, like many infection‐related genes (Breakspear et al , ; Roux et al , ; Larrainzar et al , ; van Zeijl et al , ; Damiani et al , ; Jardinaud et al , ; Liu et al , ). Within M. truncatula nodules, MtLYK10 is one of the most highly expressed LysM receptor genes, with strong expression in the distal infection zones of nodules, similarly to MtNFP and MtLYK3 (Roux et al , ; Bono et al , ).…”

Section: Discussionmentioning

confidence: 94%

Sinorhizobium meliloti succinylated high‐molecular‐weight succinoglycan and the Medicago truncatula LysM receptor‐like kinase MtLYK10 participate independently in symbiotic infection

et al. 2020

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The formation of nitrogen-fixing nodules on legume hosts is a finely tuned process involving many components of both symbiotic partners. Production of the exopolysaccharide succinoglycan by the nitrogen-fixing bacterium Sinorhizobium meliloti 1021 is needed for an effective symbiosis with Medicago spp., and the succinyl modification to this polysaccharide is critical. However, it is not known when succinoglycan intervenes in the symbiotic process, and it is not known whether the plant lysin-motif receptor-like kinase MtLYK10 intervenes in recognition of succinoglycan, as might be inferred from work on the Lotus japonicus MtLYK10 ortholog, LjEPR3. We studied the symbiotic infection phenotypes of S. meliloti mutants deficient in succinoglycan production or producing modified succinoglycan, in wild-type Medicago truncatula plants and in Mtlyk10 mutant plants. On wild-type plants, S. meliloti strains producing no succinoglycan or only unsuccinylated succinoglycan still induced nodule primordia and epidermal infections, but further progression of the symbiotic process was blocked. These S. meliloti mutants induced a more severe infection phenotype on Mtlyk10 mutant plants. Nodulation by succinoglycan-defective strains was achieved by in trans rescue with a Nod factor-deficient S. meliloti mutant. While the Nod factor-deficient strain was always more abundant inside nodules, the succinoglycan-deficient strain was more efficient than the strain producing only unsuccinylated succinoglycan. Together, these data show that succinylated succinoglycan is essential for infection thread formation in M. truncatula, and that MtLYK10 plays an important, but different role in this symbiotic process. These data also suggest that succinoglycan is more important than Nod factors for bacterial survival inside nodules.

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“…Purified LjNPL protein degrades both polygalacturonic acids and pectin. Like other mutants defective in rhizobial infection, Ljnpl mostly produced small, white, uninfected nodules Liu et al, 2019b).…”

Section: Cell Wall and Cell Membrane Componentsmentioning

confidence: 93%

“…A transposon-tagged nin mutant was defective in bacterial recognition, displaying excessive root hair curling without infection or nodulation (Schauser et al, 1999). NIN, which encodes an RWP-RK-containing TF, is a master regulator of multiple genes/processes that have positive or negative effects on nodule organogenesis, depending on the developmental time point, including IT initiation, nodule organogenesis, and the control of nodule number (Figure 4; Yano, 2008;Soyano et al, 2013Soyano et al, , 2014Liu, 2019b). NIN triggers IT initiation by inducing the LjNPL (see Cell Wall and Cell Membrane Components) and nuclear transcription factor Y subunit A-1 (MtNF-YA1) genes ( Figure 5; Xie et al, 2012;Laporte et al, 2014).…”

Section: Transcriptional Control Of Nodule Organogenesismentioning

confidence: 99%

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation

Roy¹,

Liu²,

Nandety³

et al. 2019

Plant Cell

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484

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Since 1999, various forward-and reverse-genetic approaches have uncovered nearly 200 genes required for symbiotic nitrogen fixation (SNF) in legumes. These discoveries advanced our understanding of the evolution of SNF in plants and its relationship to other beneficial endosymbioses, signaling between plants and microbes, the control of microbial infection of plant cells, the control of plant cell division leading to nodule development, autoregulation of nodulation, intracellular accommodation of bacteria, nodule oxygen homeostasis, the control of bacteroid differentiation, metabolism and transport supporting symbiosis, and the control of nodule senescence. This review catalogs and contextualizes all of the plant genes currently known to be required for SNF in two model legume species, Medicago truncatula and Lotus japonicus, and two crop species, Glycine max (soybean) and Phaseolus vulgaris (common bean). We also briefly consider the future of SNF genetics in the era of pan-genomics and genome editing.

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NIN Acts as a Network Hub Controlling a Growth Module Required for Rhizobial Infection

Cited by 109 publications

References 105 publications

Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus

Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus

Sinorhizobium meliloti succinylated high‐molecular‐weight succinoglycan and the Medicago truncatula LysM receptor‐like kinase MtLYK10 participate independently in symbiotic infection

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation

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