Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases

Symbiosis Receptor-like Kinase (SYMRK) is indispensable for the development of phosphate-acquiring arbuscular mycorrhiza (AM) as well as nitrogen-fixing root nodule symbiosis, but the mechanisms that discriminate between the two distinct symbiotic developmental fates have been enigmatic. In this study, we show that upon ectopic expression, the receptor-like kinase genes Nod Factor Receptor 1 (NFR1), NFR5, and SYMRK initiate spontaneous nodule organogenesis and nodulation-related gene expression in the absence of rhizobia. Furthermore, overexpressed NFR1 or NFR5 associated with endogenous SYMRK in roots of the legume Lotus japonicus. Epistasis tests revealed that the dominant active SYMRK allele initiates signalling independently of either the NFR1 or NFR5 gene and upstream of a set of genes required for the generation or decoding of calcium-spiking in both symbioses. Only SYMRK but not NFR overexpression triggered the expression of AM-related genes, indicating that the receptors play a key role in the decision between AM- or root nodule symbiosis-development.

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Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity

Science ◽

10.1126/science.abb3377 ◽

2020 ◽

Vol 369 (6504) ◽

pp. 663-670 ◽

Cited By ~ 4

Author(s):

Zoltan Bozsoki ◽

Kira Gysel ◽

Simon B. Hansen ◽

Damiano Lironi ◽

Christina Krönauer ◽

...

Keyword(s):

Intracellular Signaling ◽

Root Nodule ◽

Lotus Japonicus ◽

Microbial Colonization ◽

In Planta ◽

Nod Factor ◽

Differential Signaling ◽

Rhizobial Symbiosis ◽

Nodule Symbiosis ◽

Selection Of

Plants evolved lysine motif (LysM) receptors to recognize and parse microbial elicitors and drive intracellular signaling to limit or facilitate microbial colonization. We investigated how chitin and nodulation (Nod) factor receptors of Lotus japonicus initiate differential signaling of immunity or root nodule symbiosis. Two motifs in the LysM1 domains of these receptors determine specific recognition of ligands and discriminate between their in planta functions. These motifs define the ligand-binding site and make up the most structurally divergent regions in cognate Nod factor receptors. An adjacent motif modulates the specificity for Nod factor recognition and determines the selection of compatible rhizobial symbionts in legumes. We also identified how binding specificities in LysM receptors can be altered to facilitate Nod factor recognition and signaling from a chitin receptor, advancing the prospects of engineering rhizobial symbiosis into nonlegumes.

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Endogenous gibberellins affect root nodule symbiosis via transcriptional regulation of NODULE INCEPTION in Lotus japonicus

The Plant Journal ◽

10.1111/tpj.15128 ◽

2020 ◽

Author(s):

Akira Akamatsu ◽

Miwa Nagae ◽

Yuka Nishimura ◽

Daniela Romero Montero ◽

Satsuki Ninomiya ◽

...

Keyword(s):

Transcriptional Regulation ◽

Root Nodule ◽

Lotus Japonicus ◽

Root Nodule Symbiosis ◽

Nodule Symbiosis

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Intragenic Complementation of Cellulose Synthase-Like D1 alleles in Root Hair Development

10.1101/2020.03.02.973545 ◽

2020 ◽

Author(s):

Bogumil J. Karas ◽

Loretta Ross ◽

Mara Novero ◽

Lisa Amyot ◽

Sayaka Inada ◽

...

Keyword(s):

Root Hair ◽

Root Nodule ◽

Lotus Japonicus ◽

Cellulose Synthase ◽

Variable Length ◽

Root Hair Development ◽

Root Nodule Symbiosis ◽

Intragenic Complementation ◽

Hair Development ◽

Nodule Symbiosis

AbstractRoot hair cells form the primary interface of plants with the soil environment, playing key roles in nutrient uptake and plant defense. In addition, they are typically the first cells infected by nitrogen-fixing soil bacteria during the root nodule symbiosis. Here we report a role for the Cellulose Synthase-Like D1 (CSLD1) gene in root hair development in Lotus japonicus. CSLD1 belongs to the cellulose synthase protein family that includes cellulose synthases, and cellulose synthase-like proteins, the latter thought to be involved in the biosynthesis of hemicellulose. We describe 11 csld1 mutant alleles that have either short (Ljcsld1-1) or variable length roots hairs (Ljcsld1-2 to 11). Examination of Ljcsld1-1 and one variable-length root hair mutant, Ljcsld1-6 showed increased root hair cell wall thickness, which in Ljcsld1-1 was more pronounced, suggesting a possible link with the defect in root nodule symbiosis. In addition, Ljcsld1-1 heterozygotes had intermediate root hair lengths, between those of wild type and the homozygotes. Intragenic complementation was observed between alleles with mutations in the N-terminal domain and other alleles, suggesting modularity of CSLD1 function and that it may operate as a homodimer or multimer.One sentence summaryThis research describes novel gain- and loss-of-function mutations at the Lotus japonicus CELLULOSE SYNTHASE-LIKE D1 locus and analyzes their impact on root hair development.

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The role of endogenous thiamine produced via THIC in root nodule symbiosis in Lotus japonicus

Plant Science ◽

10.1016/j.plantsci.2019.03.011 ◽

2019 ◽

Vol 283 ◽

pp. 311-320

Author(s):

Yehu Yin ◽

Lu Tian ◽

Xueliu Li ◽

Mingchao Huang ◽

Leru Liu ◽

...

Keyword(s):

Root Nodule ◽

Lotus Japonicus ◽

Root Nodule Symbiosis ◽

Nodule Symbiosis

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Transcriptional regulation of NIN expression by IPN2 is required for root nodule symbiosis in Lotus japonicus

New Phytologist ◽

10.1111/nph.16553 ◽

2020 ◽

Vol 227 (2) ◽

pp. 513-528 ◽

Cited By ~ 1

Author(s):

Aifang Xiao ◽

Haixiang Yu ◽

Yuqian Fan ◽

Heng Kang ◽

Yaping Ren ◽

...

Keyword(s):

Transcriptional Regulation ◽

Root Nodule ◽

Lotus Japonicus ◽

Root Nodule Symbiosis ◽

Nodule Symbiosis

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Domain Swap Approach Reveals the Critical Roles of Different Domains of SYMRK in Root Nodule Symbiosis in Lotus japonicus

Frontiers in Plant Science ◽

10.3389/fpls.2018.00697 ◽

2018 ◽

Vol 9 ◽

Cited By ~ 3

Author(s):

Hao Li ◽

Mengxiao Chen ◽

Liujian Duan ◽

Tingting Zhang ◽

Yangrong Cao ◽

...

Keyword(s):

Root Nodule ◽

Lotus Japonicus ◽

Domain Swap ◽

Root Nodule Symbiosis ◽

Nodule Symbiosis

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Reactive Sulfur Species Interact with Other Signal Molecules in Root Nodule Symbiosis in Lotus japonicus

Antioxidants ◽

10.3390/antiox9020145 ◽

2020 ◽

Vol 9 (2) ◽

pp. 145 ◽

Cited By ~ 2

Author(s):

Mitsutaka Fukudome ◽

Hazuki Shimada ◽

Nahoko Uchi ◽

Ken-ichi Osuki ◽

Haruka Ishizaki ◽

...

Keyword(s):

Root Nodule ◽

Lotus Japonicus ◽

Signal Molecules ◽

Sulfur Species ◽

Sulfane Sulfur ◽

Root Nodule Symbiosis ◽

Infection Threads ◽

Reactive Sulfur Species ◽

Nodule Symbiosis ◽

Sulfur Donor

Reactive sulfur species (RSS) function as strong antioxidants and are involved in various biological responses in animals and bacteria. Few studies; however, have examined RSS in plants. In the present study, we clarified that RSS are involved in root nodule symbiosis in the model legume Lotus japonicus. Polysulfides, a type of RSS, were detected in the roots by using a sulfane sulfur-specific fluorescent probe, SSP4. Supplying the sulfane sulfur donor Na2S3 to the roots increased the amounts of both polysulfides and hydrogen sulfide (H2S) in the roots and simultaneously decreased the amounts of nitric oxide (NO) and reactive oxygen species (ROS). RSS were also detected in infection threads in the root hairs and in infected cells of nodules. Supplying the sulfane sulfur donor significantly increased the numbers of infection threads and nodules. When nodules were immersed in the sulfane sulfur donor, their nitrogenase activity was significantly reduced, without significant changes in the amounts of NO, ROS, and H2S. These results suggest that polysulfides interact with signal molecules such as NO, ROS, and H2S in root nodule symbiosis in L. japonicus. SSP4 and Na2S3 are useful tools for study of RSS in plants.

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