title: Adaptation of the symbiotic Mesorhizobium-chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism.
abstract: Low inorganic phosphate (Pi) availability is a major constraint for efficient nitrogen fixation in legumes, including chickpea. To elucidate the mechanisms involved in nodule acclimation to low Pi availability, two Mesorhizobium-chickpea associations exhibiting differential symbiotic performances, Mesorhizobium ciceri CP-31 (McCP-31)-chickpea and Mesorhizobium mediterranum SWRI9 (MmSWRI9)-chickpea, were comprehensively studied under both control and low Pi conditions. MmSWRI9-chickpea showed a lower symbiotic efficiency under low Pi availability than McCP-31-chickpea as evidenced by reduced growth parameters and down-regulation of nifD and nifK These differences can be attributed to decline in Pi level in MmSWRI9-induced nodules under low Pi stress, which coincided with up-regulation of several key Pi starvation-responsive genes, and accumulation of asparagine in nodules and the levels of identified amino acids in Pi-deficient leaves of MmSWRI9-inoculated plants exceeding the shoot nitrogen requirement during Pi starvation, indicative of nitrogen feedback inhibition. Conversely, Pi levels increased in nodules of Pi-stressed McCP-31-inoculated plants, because these plants evolved various metabolic and biochemical strategies to maintain nodular Pi homeostasis under Pi deficiency. These adaptations involve the activation of alternative pathways of carbon metabolism, enhanced production and exudation of organic acids from roots into the rhizosphere, and the ability to protect nodule metabolism against Pi deficiency-induced oxidative stress. Collectively, the adaptation of symbiotic efficiency under Pi deficiency resulted from highly coordinated processes with an extensive reprogramming of whole-plant metabolism. The findings of this study will enable us to design effective breeding and genetic engineering strategies to enhance symbiotic efficiency in legume crops.
authors.affiliation: Department of Biology, Lorestan University, Khorramabad 68137-17133, Iran;
authors.forename: Maryam
authors.initials: M
authors.lastname: Nasr Esfahani
authors.affiliation: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan; Metabolomics Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan;
authors.forename: Miyako
authors.initials: M
authors.lastname: Kusano
authors.affiliation: Plant Abiotic Stress Research Group and Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City 70000, Vietnam; Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan;
authors.forename: Kien Huu
authors.initials: KH
authors.lastname: Nguyen
authors.affiliation: Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan;
authors.forename: Yasuko
authors.initials: Y
authors.lastname: Watanabe
authors.affiliation: Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan;
authors.forename: Chien Van
authors.initials: CV
authors.lastname: Ha
authors.affiliation: Metabolomics Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan; Graduate School of Pharmaceutical Sciences, Chiba University, Chiba 260-8675, Japan;
authors.forename: Kazuki
authors.initials: K
authors.lastname: Saito
authors.affiliation: Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North 13314, Sudan;
authors.forename: Saad
authors.initials: S
authors.lastname: Sulieman
authors.affiliation: Laboratorio Nacional de Genómica para la Biodiversidad (Langebio)/Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados del Instituto Politécnico Nacional, 36500 Irapuato, Guanajuato, Mexico lherrera@langebio.cinvestav.mx son.tran@riken.jp.
authors.forename: Luis
authors.initials: L
authors.lastname: Herrera-Estrella
authors.affiliation: Plant Abiotic Stress Research Group and Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City 70000, Vietnam; Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan; lherrera@langebio.cinvestav.mx son.tran@riken.jp.
authors.forename: L S
authors.initials: LS
authors.lastname: Tran
mesh_terms: D000222:Adaptation, Physiological; D007887:Fabaceae / Q000378:metabolism / Q000382:microbiology*; D059128:Mesorhizobium / Q000502:physiology*; D010710:Phosphates / Q000172:deficiency / Q000378:metabolism*; D013559:Symbiosis
chemical_list: D010710:Phosphates
keywords: carbon and nitrogen metabolism; metabolomics; nitrogen fixation; phosphate deficiency; phosphate homeostasis