PLENTY, a hydroxyproline<i>O</i>-arabinosyltransferase, negatively regulates root nodule symbiosis in<i>Lotus japonicus</i>

Yoro, Emiko; Nishida, Hanna; Ogawa-Ohnishi, Mari; Yoshida, Chie; Suzaki, Takuya; Matsubayashi, Yoshikatsu; Kawaguchi, Masayoshi

doi:10.1093/jxb/ery364

Cited by 23 publications

(20 citation statements)

References 77 publications

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“…Some CLE peptides in Arabidopsis must be arabinosylated at Hyp residues in order to function (Ogawa-Ohnishi et al, 2013;Imin et al, 2018). The Mtrdn1/Ljplenty mutants, carrying a disrupted Hyp arabinosyl transferase enzyme, also hypernodulate, but unlike MtSUNN, MtRDN1 exerts its effect in roots (Yoshida et al, 2010;Schnabel et al, 2011;Yoro et al, 2019). Wild-type plants exhibit reduced nodule number in the presence of abundant available nitrogen (e.g., 10 mM KNO 3 ), but most hypernodulation mutants have nitrate-resistant nodulation, implying that nitrogen status functions as an input to AON.…”

Section: Autoregulation Of Nodulationmentioning

confidence: 99%

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

Roy¹,

Liu²,

Nandety³

et al. 2019

Plant Cell

432

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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Section: Autoregulation Of Nodulationmentioning

confidence: 99%

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

Roy¹,

Liu²,

Nandety³

et al. 2019

Plant Cell

432

484

View full text Add to dashboard Cite

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“…FIN appears to be important for arabinosylation of CLE peptides active in shoot apical meristem maintenance (Xu et al, 2015). The closest homologs in legumes have been suggested to arabinosylate some CLE peptides essential for AON (Hastwell et al, 2018;Imin et al, 2018;Kassaw et al, 2017;Yoro et al, 2019) and RDN1 is required for MtCLE53 to suppress AM colonisation in M.…”

Section: Strigolactone Levels In Fab and Fin Mutantsmentioning

confidence: 99%

“…Our understanding of AON is relatively advanced from studies in legumes including Medicago truncatula, Lotus japonicus, soybean (Glycine max) and pea (Pisum sativum). The systemic AON feedback loop begins with root events associated with nodulation inducing a specific subset of CLE peptides, some of which are tri-arabinosylated by a hydroxyproline Oarabinosyltransferase enzyme (PsNOD3, MtRDN1 and LjPLENTY) (Hastwell et al, 2018;Imin et al, 2018;Kassaw et al, 2017;Okamoto et al, 2013;Yoro et al, 2019). In L. japonicus CLE peptides are translocated to the shoot and it is clear that perception by shoot acting receptor complex(es) occurs across several species.…”

Section: Introductionmentioning

confidence: 99%

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

Wang

Velandia

Kwon

et al. 2020

Preprint

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AbstractPlants form mutualistic nutrient acquiring symbioses with microbes, including arbuscular mycorrhizal fungi. The formation of these symbioses is costly and plants employ a negative feedback loop termed autoregulation of mycorrhizae (AOM) to limit arbuscular mycorrhizae (AM) formation. We provide evidence for the role of one leucine-rich-repeat receptor like kinase (FAB), a hydroxyproline O-arabinosyltransferase enzyme (FIN), one CLE peptide, SlCLE11 and additional evidence for the one receptor like protein (SlCLV2) in the negative regulation of AM formation in tomato. Reciprocal grafting experiments suggest that the FAB gene acts locally in the root, while the SlCLV2 gene may act in both the root and the shoot. External nutrients including phosphate and nitrate can also strongly suppress AM formation. We found that FAB and FIN are required for nitrate suppression of AM but are not required for the powerful suppression of AM colonisation by phosphate. This parallels some of the roles of legume homologs in the autoregulation of the more recently evolved symbioses with nitrogen-fixing bacteria leading to nodulation. This deep homology in the symbiotic role of these genes suggests that in addition to the early signalling events that lead to the establishment of AM and nodulation, the autoregulation pathway might also be considered part of the common symbiotic toolkit that enabled plants to form beneficial symbioses.HighlightWe describe the role of CLV signalling elements in the negative regulation of arbuscular mycorrhizal symbioses of tomato, including influencing nitrate but not phosphate suppression of mycorrhizal colonisation.

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“…In L. japonicus , tri-arabinosylation of CLE-RS2 peptide is required for the direct binding of HAR1 and suppression of nodulation in a HAR1-dependent manner 5 . Moreover, the inhibitory effects of CLE peptides on nodulation in L. japonicus depend partially on the gene known as PLENTY , which encodes hydroxyproline‐O‐arabinosyl transferase (HPAT) 26 . In M. truncatula , mutants of ROOT DETERMINED NODULATION1 27 , 28 , an orthologous gene to PLENTY , show a similar phenotype to plenty .…”

Section: Introductionmentioning

confidence: 99%

MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus

et al. 2020

Self Cite

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Legumes utilize a shoot-mediated signaling system to maintain a mutualistic relationship with nitrogen-fixing bacteria in root nodules. In Lotus japonicus, shoot-to-root transfer of microRNA miR2111 that targets TOO MUCH LOVE, a nodulation suppressor in roots, has been proposed to explain the mechanism underlying nodulation control from shoots. However, the role of shoot-accumulating miR2111s for the systemic regulation of nodulation was not clearly shown. Here, we find L. japonicus has seven miR2111 loci, including those mapped through RNA-seq. MIR2111-5 expression in leaves is the highest among miR2111 loci and repressed after rhizobial infection depending on a shoot-acting HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor. MIR2111-5 knockout mutants show significantly decreased nodule numbers and miR2111 levels. Furthermore, grafting experiments using transformants demonstrate scions with altered miR2111 levels influence nodule numbers in rootstocks in a dose-dependent manner. Therefore, miR2111 accumulation in leaves through MIR2111-5 expression is required for HAR1-dependent systemic optimization of nodule number.

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PLENTY, a hydroxyprolineO-arabinosyltransferase, negatively regulates root nodule symbiosis inLotus japonicus

Abstract: The gene responsible for the plenty hypernodulation phenotype in Lotus japonicus was identified. The enzymatic activity and Golgi localization of PLENTY demonstrated its function as a post-translational modification enzyme.

Cited by 23 publications

References 77 publications

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

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

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus

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