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Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus

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  • Jieshun Lin

    (Aarhus University)

  • Yuda Purwana Roswanjaya

    (Wageningen University
    Agency for the Assessment and Application of Technology (BPPT))

  • Wouter Kohlen

    (Wageningen University)

  • Jens Stougaard

    (Aarhus University)

  • Dugald Reid

    (Aarhus University)

Abstract

Legumes balance nitrogen acquisition from soil nitrate with symbiotic nitrogen fixation. Nitrogen fixation requires establishment of a new organ, which is a cytokinin dependent developmental process in the root. We found cytokinin biosynthesis is a central integrator, balancing nitrate signalling with symbiotic acquired nitrogen. Low nitrate conditions provide a permissive state for induction of cytokinin by symbiotic signalling and thus nodule development. In contrast, high nitrate is inhibitory to cytokinin accumulation and nodule establishment in the root zone susceptible to nodule formation. This reduction of symbiotic cytokinin accumulation was further exacerbated in cytokinin biosynthesis mutants, which display hypersensitivity to nitrate inhibition of nodule development, maturation and nitrogen fixation. Consistent with this, cytokinin application rescues nodulation and nitrogen fixation of biosynthesis mutants in a concentration dependent manner. These inhibitory impacts of nitrate on symbiosis occur in a Nlp1 and Nlp4 dependent manner and contrast with the positive influence of nitrate on cytokinin biosynthesis that occurs in species that do not form symbiotic root nodules. Altogether this shows that legumes, as exemplified by Lotus japonicus, have evolved a different cytokinin response to nitrate compared to non-legumes.

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  • Jieshun Lin & Yuda Purwana Roswanjaya & Wouter Kohlen & Jens Stougaard & Dugald Reid, 2021. "Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26820-9
    DOI: 10.1038/s41467-021-26820-9
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    1. Xin Wang & Zhimin Qiu & Wenjun Zhu & Nan Wang & Mengyan Bai & Huaqin Kuang & Chenlin Cai & Xiangbin Zhong & Fanjiang Kong & Peitao Lü & Yuefeng Guan, 2023. "The NAC transcription factors SNAP1/2/3/4 are central regulators mediating high nitrogen responses in mature nodules of soybean," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Ke Tao & Ib T. Jensen & Sha Zhang & Eber Villa-Rodríguez & Zuzana Blahovska & Camilla Lind Salomonsen & Anna Martyn & Þuríður Nótt Björgvinsdóttir & Simon Kelly & Luc Janss & Marianne Glasius & Rasmus, 2024. "Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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