TOO MUCH LOVE, a Novel Kelch Repeat-Containing F-box Protein, Functions in the Long-Distance Regulation of the Legume–Rhizobium Symbiosis

Takahara, Masahiro; Magori, Shimpei; Soyano, Takashi; Okamoto, Satoru; Yoshida, Chie; Yano, Koji; Sato, Shusei; Tabata, Satoshi; Yamaguchi, Katsushi; Shigenobu, Shuji; Takeda, Nobuo; Suzaki, Takuya; Kawaguchi, Masayoshi

doi:10.1093/pcp/pct022

Cited by 121 publications

(127 citation statements)

References 74 publications

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“…We used two L. japonicus accessions, Gifu B-129 and MG-20, as the WT, along with five symbiotic mutants, nin-2, hit1, har1-7, tml-1, and tml-4 (15,19,23,41). Unless stated otherwise in a figure legend, MG-20 served as the WT.…”

Section: Methodsmentioning

confidence: 99%

“…TML encodes an F-box protein that acts downstream of HAR1 in the root (23). CLE-RS1 and CLE-RS2 suppress nodulation in an HAR1-and TML-dependent fashion (11,23); har1 and tml mutants produce excessive numbers of nodules because AON is not operational. To investigate whether the systemic effects of NIN-GR are related to activation of AON, we introduced Pro35S-NIN-GR into roots of har1-7 and tml-1 mutants, as well as WT plants.…”

Section: Nin Ectopic Expression Systemically Suppresses Nodulation Thmentioning

confidence: 99%

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NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Soyano

Hirakawa

Sato

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Autoregulatory negative-feedback loops play important roles in finebalancing tissue and organ development. Such loops are composed of short-range intercellular signaling pathways via cell-cell communications. On the other hand, leguminous plants use a long-distance negative-feedback system involving root-shoot communication to control the number of root nodules, root lateral organs that harbor symbiotic nitrogen-fixing bacteria known as rhizobia. This feedback system, known as autoregulation of nodulation (AON), consists of two long-distance mobile signals: root-derived and shoot-derived signals. Two Lotus japonicus CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE)-related small peptides, CLE ROOT SIGNAL1 (CLE-RS1) and CLE-RS2, function as root-derived signals and are perceived by a shoot-acting AON factor, the HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor protein, an ortholog of Arabidopsis CLAVATA1, which is responsible for shoot apical meristem homeostasis. This peptide-receptor interaction is necessary for systemic suppression of nodulation. How the onset of nodulation activates AON and how optimal nodule numbers are maintained remain unknown, however. Here we show that an RWP-RK-containing transcription factor, NODULE INCEPTION (NIN), which induces nodule-like structures without rhizobial infection when expressed ectopically, directly targets CLE-RS1 and CLE-RS2. Roots constitutively expressing NIN systemically repress activation of endogenous NIN expression in untransformed roots of the same plant in a HAR1-dependent manner, leading to systemic suppression of nodulation and down-regulation of CLE expression. Our findings provide, to our knowledge, the first molecular evidence of a long-distance autoregulatory negative-feedback loop that homeostatically regulates nodule organ formation.L ong-distance organ-to-organ communications are generally critical for coordinating development and environmental adaptation in multicellular organisms, particularly plants that continuously produce postembryonic organs in various environmental conditions (1, 2). Autoregulatory negative-feedback loops play important roles in fine-balancing tissue and organ development. Such feedback loops include short-range intercellular signaling via cell-cell communication. In Arabidopsis, shoot apical meristem (SAM) regulation involves a well-characterized short-range negative-feedback loop that maintains the homeostasis of plant organ development (3-6). The molecular substance of long-distance negative-feedback loops that homeostatically regulate organ production and development remains largely unknown, however.Leguminous plants use long-distance autoregulatory negativefeedback systems involving root-shoot communications to control the number of root nodules, symbiotic root lateral organs formed as consequence of successful interaction with nitrogenfixing bacteria, collectively known as rhizobia. This nodule symbiosis is beneficial to host plants, because rhizobia accommodated in nodules convert atmospheric nitrogen to ammonium, a ...

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Section: Methodsmentioning

confidence: 99%

Section: Nin Ectopic Expression Systemically Suppresses Nodulation Thmentioning

confidence: 99%

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Soyano

Hirakawa

Sato

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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189

200

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“…However, the underlying mechanisms remain obscure. KISS ME DEADLY, a Kelch repeat F-box protein that resembles TML, acts as a negative regulator of CK signalling in Arabidopsis 19,48 . Thus, interactions between CKs and TML may be essential for the negative regulation of nodulation, as well as lateral root development by CKs.…”

Section: Expression Analyses Of L Japonicus Ipt Genes In Shootsmentioning

confidence: 99%

Shoot-derived cytokinins systemically regulate root nodulation

et al. 2014

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Legumes establish symbiotic associations with nitrogen-fixing bacteria (rhizobia) in root nodules to obtain nitrogen. Legumes control nodule number through long-distance communication between roots and shoots, maintaining the proper symbiotic balance. Rhizobial infection triggers the production of mobile CLE-RS1/2 peptides in Lotus japonicus roots; the perception of the signal by receptor kinase HAR1 in shoots presumably induces the production of an unidentified shoot-derived inhibitor (SDI) that translocates to roots and blocks further nodule development. Here we show that, CLE-RS1/2-HAR1 signalling activates the production of shoot-derived cytokinins, which have an SDI-like capacity to systemically suppress nodulation. In addition, we show that LjIPT3 is involved in nodulation-related cytokinin production in shoots. The expression of LjIPT3 is activated in an HAR1-dependent manner. We further demonstrate shoot-to-root long-distance transport of cytokinin in L. japonicus seedlings. These findings add essential components to our understanding of how legumes control nodulation to balance nutritional requirements and energy status.

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“…CLE peptide dependent nodule regulation in L. japonicus requires the LRR receptor kinase HYPERNODULATION AND ABERRANT ROOT1 (HAR1) and induces ISO-PENTENYL TRANSFERASE (IPT3) dependent cytokinin biosynthesis in the shoot, which negatively regulates nodulation (Krusell et al, 2002;Nishimura et al, 2002;Okamoto et al, 2013;Sasaki et al, 2014). LHK1 was not required for this negative regulatory role of cytokinin, but it was dependent on the function of the Kelch repeat-containing F-box protein, TOO MUCH LOVE in the root (Takahara et al, 2013;Sasaki et al, 2014).…”

mentioning

confidence: 99%

CYTOKININ OXIDASE/DEHYDROGENASE3 Maintains Cytokinin Homeostasis during Root and Nodule Development in Lotus japonicus

et al. 2015

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Cytokinins are required for symbiotic nodule development in legumes, and cytokinin signaling responses occur locally in nodule primordia and in developing nodules. Here, we show that the Lotus japonicus Ckx3 cytokinin oxidase/dehydrogenase gene is induced by Nod factor during the early phase of nodule initiation. At the cellular level, pCkx3::YFP reporter-gene studies revealed that the Ckx3 promoter is active during the first cortical cell divisions of the nodule primordium and in growing nodules. Cytokinin measurements in ckx3 mutants confirmed that CKX3 activity negatively regulates root cytokinin levels. Particularly, tZ and DHZ type cytokinins in both inoculated and uninoculated roots were elevated in ckx3 mutants, suggesting that these are targets for degradation by the CKX3 cytokinin oxidase/dehydrogenase. The effect of CKX3 on the positive and negative roles of cytokinin in nodule development, infection and regulation was further clarified using ckx3 insertion mutants. Phenotypic analysis indicated that ckx3 mutants have reduced nodulation, infection thread formation and root growth. We also identify a role for cytokinin in regulating nodulation and nitrogen fixation in response to nitrate as ckx3 phenotypes are exaggerated at increased nitrate levels. Together, these findings show that cytokinin accumulation is tightly regulated during nodulation in order to balance the requirement for cell divisions with negative regulatory effects of cytokinin on infection events and root development.

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TOO MUCH LOVE, a Novel Kelch Repeat-Containing F-box Protein, Functions in the Long-Distance Regulation of the Legume–Rhizobium Symbiosis

Cited by 121 publications

References 74 publications

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Shoot-derived cytokinins systemically regulate root nodulation

CYTOKININ OXIDASE/DEHYDROGENASE3 Maintains Cytokinin Homeostasis during Root and Nodule Development in Lotus japonicus

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