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Intragenic complementation at the Lotus japonicus CELLULOSE SYNTHASE-LIKE D1 locus rescues root hair defects.

ABSTRACT: Root hair cells form the primary interface of plants with the soil environment, playing key roles in nutrient uptake and plant defense. In legumes, they are typically the first cells to become infected by nitrogen-fixing soil bacteria during root nodule symbiosis. Here, we report a role for the CELLULOSE SYNTHASE-LIKE D1 (CSLD1) gene in root hair development in the legume species 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 Ljcsld1 mutant alleles that impose either short (Ljcsld1-1) or variable (Ljcsld1-2 to 11) root hair length phenotypes. Examination of Ljcsld1-1 and one variable-length root hair mutant, Ljcsld1-6, revealed increased root hair cell wall thickness, which in Ljcsld1-1 was significantly more pronounced and also associated with a strong defect in root nodule symbiosis. Lotus japonicus plants heterozygous for Ljcsld1-1 exhibited intermediate root hair lengths, suggesting incomplete dominance. Intragenic complementation was observed between alleles with mutations in different CSLD1 domains, suggesting CSLD1 function is modular and that the protein may operate as a homodimer or multimer during root hair development.

SUBMITTER: Karas BJ

PROVIDER: S-EPMC8331140 | biostudies-literature |

REPOSITORIES: biostudies-literature

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The karrikin signaling regulator SMAX1 controls <i>Lotus japonicus</i> root and root hair development by suppressing ethylene biosynthesis.

Project description:An evolutionarily ancient plant hormone receptor complex comprising the α/β-fold hydrolase receptor KARRIKIN INSENSITIVE 2 (KAI2) and the F-box protein MORE AXILLARY GROWTH 2 (MAX2) mediates a range of developmental responses to smoke-derived butenolides called karrikins (KARs) and to yet elusive endogenous KAI2 ligands (KLs). Degradation of SUPPRESSOR OF MAX2 1 (SMAX1) after ligand perception is considered to be a key step in KAR/KL signaling. However, molecular events which regulate plant development downstream of SMAX1 removal have not been identified. Here we show that Lotus japonicus SMAX1 is specifically degraded in the presence of KAI2 and MAX2 and plays an important role in regulating root and root hair development. smax1 mutants display very short primary roots and elongated root hairs. Their root transcriptome reveals elevated ethylene responses and expression of ACC Synthase 7 (ACS7), which encodes a rate-limiting enzyme in ethylene biosynthesis. smax1 mutants release increased amounts of ethylene and their root phenotype is rescued by treatment with ethylene biosynthesis and signaling inhibitors. KAR treatment induces ACS7 expression in a KAI2-dependent manner and root developmental responses to KAR treatment depend on ethylene signaling. Furthermore, in Arabidopsis, KAR-induced root hair elongation depends on ACS7 Thus, we reveal a connection between KAR/KL and ethylene signaling in which the KAR/KL signaling module (KAI2-MAX2-SMAX1) regulates the biosynthesis of ethylene to fine-tune root and root hair development, which are important for seedling establishment at the beginning of the plant life cycle.

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SNARE Proteins LjVAMP72a and LjVAMP72b Are Required for Root Symbiosis and Root Hair Formation in <i>Lotus japonicus</i>.

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Dataset Lotus Japonicus root exudates

Project description:The present dataset is composed of Lotus japonicus root exudate samples under different nitrogen states: starved (no nitrogen), inorganic N (KNO3), symbiotic N (inoculation with M. loti), and inorganic/symbiotic (KNO3 + M. loti). The samples were analyzed by ultra-high-performance liquid chromatography (UHPLC) coupled to a quadrupole time-of-flight mass spectrometer (qToF MS, Bruker Compact) with electrospray ionization.

2023-05-22 | MSV000092000 | MassIVE

Early Lotus japonicus root transcriptomic responses to symbiotic and pathogenic fungal exudates.

Project description:The objective of this study is to evaluate Lotus japonicus transcriptomic responses to arbuscular mycorrhizal (AM) germinated spore exudates (GSEs), responsible for activating nuclear Ca(2+) spiking in plant root epidermis. A microarray experiment was performed comparing gene expression in Lotus rootlets treated with GSE or water after 24 and 48 h. The transcriptional pattern of selected genes that resulted to be regulated in the array was further evaluated upon different treatments and timings. In particular, Lotus rootlets were treated with: GSE from the pathogenic fungus Colletotrichum trifolii; short chitin oligomers (COs; acknowledged AM fungal signals) and long COs (as activators of pathogenic responses). This experimental set up has revealed that AM GSE generates a strong transcriptomic response in Lotus roots with an extensive defense-related response after 24 h and a subsequent down-regulation after 48 h. A similar subset of defense-related genes resulted to be up-regulated also upon treatment with C. trifolii GSE, although with an opposite trend. Surprisingly, long COs activated both defense-like and symbiosis-related genes. Among the genes regulated in the microarray, promoter-GUS assay showed that LjMATE1 activates in epidermal cells and root hairs.

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LAZY3 plays a pivotal role in positive root gravitropism in Lotus japonicus.

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Nitric Oxide Detoxification by Mesorhizobium loti Affects Root Nodule Symbiosis with Lotus japonicus.

Project description:Root nodule symbiosis between legumes and rhizobia involves nitric oxide (NO) regulation by both the host plant and symbiotic rhizobia. However, the mechanisms by which the rhizobial control of NO affects root nodule symbiosis in Lotus japonicus are unknown. Therefore, we herein investigated the effects of enhanced NO removal by Mesorhizobium loti on symbiosis with L. japonicus. The hmp gene, which in Sinorhizobium meliloti encodes a flavohemoglobin involved in NO detoxification, was introduced into M. loti to generate a transconjugant with enhanced NO removal. The symbiotic phenotype of the transconjugant with L. japonicus was examined. The transconjugant showed delayed infection and higher nitrogenase activity in mature nodules than the wild type, whereas nodule senescence was normal. This result is in contrast to previous findings showing that enhanced NO removal in L. japonicus by class 1 phytoglobin affected nodule senescence. To evaluate differences in NO detoxification between M. loti and L. japonicus, NO localization in nodules was investigated. The enhanced expression of class 1 phytoglobin in L. japonicus reduced the amount of NO not only in infected cells, but also in vascular bundles, whereas that of hmp in M. loti reduced the amount of NO in infected cells only. This difference suggests that NO detoxification by M. loti exerts different effects in symbiosis than that by L. japonicus.

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PLENTY, a hydroxyproline O-arabinosyltransferase, negatively regulates root nodule symbiosis in Lotus japonicus.

Project description:Legumes can survive in nitrogen-deficient environments by forming root-nodule symbioses with rhizobial bacteria; however, forming nodules consumes energy, and nodule numbers must thus be strictly controlled. Previous studies identified major negative regulators of nodulation in Lotus japonicus, including the small peptides CLAVATA3/ESR (CLE)-RELATED-ROOT SIGNAL1 (CLE-RS1), CLE-RS2, and CLE-RS3, and their putative major receptor HYPERNODULATION AND ABERRANT ROOT FORMATION1 (HAR1). CLE-RS2 is known to be expressed in rhizobia-inoculated roots, and is predicted to be post-translationally arabinosylated, a modification essential for its activity. Moreover, all three CLE-RSs suppress nodulation in a HAR1-dependent manner. Here, we identified PLENTY as a gene responsible for the previously isolated hypernodulation mutant plenty. PLENTY encoded a hydroxyproline O-arabinosyltransferase orthologous to ROOT DETERMINED NODULATION1 in Medicago truncatula. PLENTY was localized to the Golgi, and an in vitro analysis of the recombinant protein demonstrated its arabinosylation activity, indicating that CLE-RS1/2/3 may be substrates for PLENTY. The constitutive expression experiments showed that CLE-RS3 was the major candidate substrate for PLENTY, suggesting the substrate preference of PLENTY for individual CLE-RS peptides. Furthermore, a genetic analysis of the plenty har1 double mutant indicated the existence of another PLENTY-dependent and HAR1-independent pathway negatively regulating nodulation.

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Transcriptomic Changes in Medicago truncatula and Lotus japonicus Root Nodules during Drought Stress.

Project description:Drought is one of the major environmental factors limiting biomass and seed yield production in agriculture. In this research, we focused on plants from the Fabaceae family, which has a unique ability for the establishment of symbiosis with nitrogen-fixing bacteria, and are relatively susceptible to water limitation. We have presented the changes in nitrogenase activity and global gene expression occurring in Medicagotruncatula and Lotusjaponicus root nodules during water deficit. Our results proved a decrease in the efficiency of nitrogen fixation, as well as extensive changes in plant and bacterial transcriptomes, shortly after watering cessation. We showed for the first time that not only symbiotic plant components but also Sinorhizobiummeliloti and Mesorhizobiumloti bacteria residing in the root nodules of M. truncatula and L. japonicus, respectively, adjust their gene expression in response to water shortage. Although our results demonstrated that both M. truncatula and L.japonicus root nodules were susceptible to water deprivation, they indicated significant differences in plant and bacterial response to drought between the tested species, which might be related to the various types of root nodules formed by these species.

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Expression Analysis of PIN Genes in Root Tips and Nodules of Lotus japonicus.

Project description:Auxins are postulated to be one of the pivotal factors in nodulation. However, their transporters in Lotus japonicus, the model species for the study of the development of determinate-type root nodules, have been scarcely described so far, and thus their role in nodulation has remained unknown. Our research is the first focusing on polar auxin transporters in L. japonicus. We analyzed and compared expression of PINs in 20 days post rhizobial inoculation (dpi) and 54 dpi root nodules of L. japonicus by real-time quantitative polymerase chain reaction (qPCR) along with the histochemical β-glucuronidase (GUS) reporter gene assay in transgenic hairy roots. The results indicate that LjPINs are essential during root nodule development since they are predominantly expressed in the primordia and young, developing nodules. However, along with differentiation, expression levels of several PINs decreased and occurred particularly in the nodule vascular bundles, especially in connection with the root's stele. Moreover, our study demonstrated the importance of both polar auxin transport and auxin intracellular homeostasis during L. japonicus root nodule development and differentiation.

| S-EPMC6359356 | biostudies-literature

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities.

Project description:Lotus japonicus has been used for decades as a model legume to study the establishment of binary symbiotic relationships with nitrogen-fixing rhizobia that trigger root nodule organogenesis for bacterial accommodation. Using community profiling of 16S rRNA gene amplicons, we reveal that in Lotus, distinctive nodule- and root-inhabiting communities are established by parallel, rather than consecutive, selection of bacteria from the rhizosphere and root compartments. Comparative analyses of wild-type (WT) and symbiotic mutants in Nod factor receptor5 (nfr5), Nodule inception (nin) and Lotus histidine kinase1 (lhk1) genes identified a previously unsuspected role of the nodulation pathway in the establishment of different bacterial assemblages in the root and rhizosphere. We found that the loss of nitrogen-fixing symbiosis dramatically alters community structure in the latter two compartments, affecting at least 14 bacterial orders. The differential plant growth phenotypes seen between WT and the symbiotic mutants in nonsupplemented soil were retained under nitrogen-supplemented conditions that blocked the formation of functional nodules in WT, whereas the symbiosis-impaired mutants maintain an altered community structure in the nitrogen-supplemented soil. This finding provides strong evidence that the root-associated community shift in the symbiotic mutants is a direct consequence of the disabled symbiosis pathway rather than an indirect effect resulting from abolished symbiotic nitrogen fixation. Our findings imply a role of the legume host in selecting a broad taxonomic range of root-associated bacteria that, in addition to rhizobia, likely contribute to plant growth and ecological performance.

| S-EPMC5150415 | biostudies-literature

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