Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots

Imaizumi-Anraku, Haruko; Takeda, Nobuo; Charpentier, Myriam; Perry, Jillian; Miwa, Hiroki; Umehara, Yosuke; Kouchi, Hiroshi; Murakami, Yasuhiro; Mulder, Lonneke; Vickers, Kate; Pike, Jodie; Downie, J. Allan; Wang, Trevor; Sato, Shusei; Asamizu, Erika; Tabata, Satoshi; Yoshikawa, Makoto; Murooka, Yoshikatsu; Wu, Guo Jiang; Kawaguchi, Masayoshi; Kawasaki, Shinji; Parniske, Martin; Hayashi, Makoto

doi:10.1038/nature03237

Cited by 368 publications

(247 citation statements)

References 29 publications

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“…The putative cation channel DMI1 may have a direct role in calcium spiking, in that it could function as a calcium channel during both the calcium flux and calcium spiking. However, two proteins homologous to DMI1, CASTOR and POLLUX, have recently been identified in L. japonicus that are required for Nod factor signaling and show plastid localization (Imaizumi-Anraku et al, 2005). The plastid is an unlikely internal calcium store for calcium spiking, and, therefore, this localization suggests that this class of putative cation channels is not the calcium channel involved in calcium spiking.…”

Section: Nod Factor Signalingmentioning

confidence: 99%

Peace Talks and Trade Deals. Keys to Long-Term Harmony in Legume-Microbe Symbioses

2005

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Section: Nod Factor Signalingmentioning

confidence: 99%

Peace Talks and Trade Deals. Keys to Long-Term Harmony in Legume-Microbe Symbioses

2005

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“…The transcript abundance of this gene represents a useful indicator for the activity of Nod factor signal transduction, because mutations that block the Nod factorinduced signaling pathway in L. japonicus block NIN induction Imaizumi-Anraku et al, 2005;Miwa et al, 2006b;Marsh et al, 2007). NIN induction was observed in roots of wild-type plants and in the vector control line 24 and 48 h after Nod factor treatment (Fig.…”

Section: Lnp Is Required For Nod Factor Induction Of Nodule Inceptionmentioning

confidence: 99%

“…The POLYUBIQUITIN gene was used as an internal positive control. Forward and reverse primers used were as follows: NIN, 59-CCAAGCAGCAGTGAATGAGA-39 and 59-AGG-AGCCCAAGTGAGTGCTA-39; LNP, 59-TTGGTGGGATATGGAATGGT-39 and 59-TGGCATTGGGTTTATTCACA-39; LNP2, 59-TGGGTCAAGCTTAA-ACGAATG-39 and 59-CCCTCCACCATTCCATATACC-39; POLYUBIQUITIN, 59-ATGCAGATCTTCGTCAAGACCTTGAC-39 and 59-ACCTCCCCTCAGA-CGAAGGA-39 (Imaizumi-Anraku et al, 2005). In order to avoid the amplification of the antisense LNP RNA when quantifying the transcript levels, LNP primers were designed using a 39 region that was absent from the 59D antisense vector.…”

Section: Expression Analysismentioning

confidence: 99%

“…At the core of this common symbiosis signaling (SYM) pathway are oscillations in nucleusassociated cytosolic calcium levels, termed calcium spiking, acting as a secondary messenger to induce gene expression. A receptor-like kinase (SYMRK/DMI2 [Endre et al, 2002;Stracke et al, 2002]), three components of the nuclear pore (NUP133, NUP85, and NENA [Kanamori et al, 2006;Saito et al, 2007;Groth et al, 2010]), and nucleus-localized cation channels (POLLUX/ DMI1, CASTOR Imaizumi-Anraku et al, 2005;Charpentier et al, 2008]) are all required for the induction of calcium spiking, while a calciumand calmodulin-dependent protein kinase (CCaMK Mitra et al, 2004;Tirichine et al, 2006]) and a protein of unknown function (CYCLOPS/ IPD3 [Messinese et al, 2007;Yano et al, 2008]) are necessary for perception of the calcium signal and the induction of downstream genes. In addition to the common symbiosis pathway, Nod factor signaling also involves the nodulation-specific receptor-like kinases NFR1/LYK3 and NFR5/NFP (Limpens et al, 2003;Madsen et al, 2003;Radutoiu et al, 2003;Arrighi et al, 2006) that appear to function in Nod factor perception.…”

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confidence: 99%

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Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling

Morieri

Kalsi

et al. 2012

Plant Physiology

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(J.S., P.M.G.)Nodulation in legumes requires the recognition of rhizobially made Nod factors. Genetic studies have revealed that the perception of Nod factors involves LysM domain receptor-like kinases, while biochemical approaches have identified LECTIN NUCLEOTIDE PHOSPHOHYDROLASE (LNP) as a Nod factor-binding protein. Here, we show that antisense inhibition of LNP blocks nodulation in Lotus japonicus. This absence of nodulation was due to a defect in Nod factor signaling based on the observations that the early nodulation gene NODULE INCEPTION was not induced and that both Nod factor-induced perinuclear calcium spiking and calcium influx at the root hair tip were blocked. However, Nod factor did induce root hair deformation in the LNP antisense lines. LNP is also required for infection by the mycorrhizal fungus Glomus intraradices, suggesting that LNP plays a role in the common signaling pathway shared by the rhizobial and mycorrhizal symbioses. Taken together, these observations indicate that LNP acts at a novel position in the early stages of symbiosis signaling. We propose that LNP functions at the earliest stage of the common nodulation and mycorrhization symbiosis signaling pathway downstream of the Nod factor receptors; it may act either by influencing signaling via changes in external nucleotides or in conjunction with the LysM receptor-like kinases for recognition of Nod factor.

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“…The genetic requirements for rhizobial and arbuscular mycorrhizal (AM) fungal interactions in plants overlap in a common symbiosis pathway (CSP) that leads to successful root nodule (RN) and AM symbioses (21,24,46). Similarly, the negative control of the degree of nodulation and mycorrhization of roots is also regulated through a common signaling system, so-called autoregulation of nodulation (42).…”

Section: The Effects Of the Oryza Sativa Calcium/calmodulin-dependentmentioning

confidence: 99%

The Genotype of the Calcium/Calmodulin-Dependent Protein Kinase Gene ( CCaMK ) Determines Bacterial Community Diversity in Rice Roots under Paddy and Upland Field Conditions

Ikeda

Okubo

Takeda

et al. 2011

Appl Environ Microbiol

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The effects of the Oryza sativa calcium/calmodulin-dependent protein kinase OsCCaMK genotype (dominant homozygous [D], heterozygous [H], recessive homozygous [R]) on rice root-associated bacteria, including endophytes and epiphytes, were examined by using a Tos17 rice mutant line under paddy and upland field conditions. Roots were sampled at the flowering stage and were subjected to clone library analyses. The relative abundance of Alphaproteobacteria was noticeably decreased in R plants under both paddy and upland conditions (0.8% and 3.0%, respectively) relative to those in D plants (10.3% and 17.4%, respectively). Population shifts of the Sphingomonadales and Rhizobiales were mainly responsible for this low abundance in R plants. The abundance of Anaerolineae (Chloroflexi) and Clostridia (Firmicutes) was increased in R plants under paddy conditions. The abundance of a subpopulation of Actinobacteria (Saccharothrix spp. and unclassified Actinosynnemataceae) was increased in R plants under upland conditions. Principal coordinate analysis revealed unidirectional community shifts in relation to OsCCaMK gene dosage under both conditions. In addition, shoot length, tiller number, and plant weight decreased as the OsCCaMK gene dosage decreased under upland conditions. These results suggest significant impacts of OsCCaMK on both the diversity of root-associated bacteria and rice plant growth under both paddy and upland field conditions.Legumes developed systems to attain mutual symbiosis with rhizobia and mycorrhizae during their evolution. The genetic requirements for rhizobial and arbuscular mycorrhizal (AM) fungal interactions in plants overlap in a common symbiosis pathway (CSP) that leads to successful root nodule (RN) and AM symbioses (21,24,46). Similarly, the negative control of the degree of nodulation and mycorrhization of roots is also regulated through a common signaling system, so-called autoregulation of nodulation (42). These findings raise the question of whether molecular components regulating RN and AM symbioses also affect other symbiotic microbes in the phytosphere.Diverse microorganisms reside in and on plants as endophytes and epiphytes (11,29,35,48). These symbiotic microbes assist plants in the uptake of nutrients (22), scavenge toxic compounds (5), and exert considerable influence upon the overall health of host plants (6). However, many questions remain about the driving forces and ecological rules underlying the relationships between these microbes and plants (12,36).Recently, it was shown that symbiosis-defective mutants of Medicago truncatula (30) and soybean (16, 32) possess bacterial and fungal communities in their roots different from those in wild-type host plants and that certain bacteria preferentially associate with mycorrhizal roots (41). These findings indicate that genetic alteration in RN/AM signaling pathways can also alter the microflora of the rhizosphere. Interestingly, analyses of the rhizosphere of soybeans indicated that the bacterial community structures of nonnodulated...

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Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots

Cited by 368 publications

References 29 publications

Peace Talks and Trade Deals. Keys to Long-Term Harmony in Legume-Microbe Symbioses

Peace Talks and Trade Deals. Keys to Long-Term Harmony in Legume-Microbe Symbioses

Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling

The Genotype of the Calcium/Calmodulin-Dependent Protein Kinase Gene ( CCaMK ) Determines Bacterial Community Diversity in Rice Roots under Paddy and Upland Field Conditions

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