Antiquity and Function of<i>CASTOR</i>and<i>POLLUX</i>, the Twin Ion Channel-Encoding Genes Key to the Evolution of Root Symbioses in Plants

Chen, Caiyan; Fan, Cui; Gao, Muqiang; Zhu, Hongyan

doi:10.1104/pp.108.131540

Cited by 65 publications

(43 citation statements)

References 94 publications

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“…These observations are further supported by the inability of rice POLLUX to rescue dmi1 when expressed alone, in which only bumps devoid of bacteria were observed (Chen et al, 2009). By contrast, pea SYM8 could rescue not only dmi1 (Edwards et al, 2007), but also Lj-castor, Lj-pollux, and the Lj-castor pollux double mutant of L. japonicus, just like DMI1 (this study).…”

Section: Discussionsupporting

confidence: 71%

“…These DMI1 homologs are present throughout land plants and represent ancient innovations that probably allowed the development of the AM symbiosis and colonization of land by plants (Zhu et al, 2006;Wang et al, 2010). Consistent with the phylogenetically widespread occurrence of common symbiosis genes and AM, rice (Oryza sativa) putative orthologs Os-CASTOR and Os-POLLUX are required for the AM symbiosis Gutjahr et al, 2008;Chen et al, 2009). The presence of a POLLUX putative ortholog in Arabidopsis thaliana is intriguing, as Arabidopsis does not undergo mycorrhization.…”

Section: Introductionmentioning

confidence: 97%

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The Recent Evolution of a Symbiotic Ion Channel in the Legume Family Altered Ion Conductance and Improved Functionality in Calcium Signaling

et al. 2012

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Arbuscular mycorrhiza and the rhizobia-legume symbiosis are two major root endosymbioses that facilitate plant nutrition. In Lotus japonicus, two symbiotic cation channels, CASTOR and POLLUX, are indispensable for the induction of nuclear calcium spiking, one of the earliest plant responses to symbiotic partner recognition. During recent evolution, a single amino acid substitution in DOES NOT MAKE INFECTIONS1 (DMI1), the POLLUX putative ortholog in the closely related Medicago truncatula, rendered the channel solo sufficient for symbiosis; castor, pollux, and castor pollux double mutants of L. japonicus were rescued by DMI1 alone, while both Lj-CASTOR and Lj-POLLUX were required for rescuing a dmi1 mutant of M. truncatula. Experimental replacement of the critical serine by an alanine in the selectivity filter of Lj-POLLUX conferred a symbiotic performance indistinguishable from DMI1. Electrophysiological characterization of DMI1 and Lj-CASTOR (wildtype and mutants) by planar lipid bilayer experiments combined with calcium imaging in Human Embryonic Kidney-293 cells expressing DMI1 (the wild type and mutants) suggest that the serine-to-alanine substitution conferred reduced conductance with a long open state to DMI1 and improved its efficiency in mediating calcium oscillations. We propose that this single amino acid replacement in the selectivity filter made DMI1 solo sufficient for symbiosis, thus explaining the selective advantage of this allele at the mechanistic level.

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Section: Discussionsupporting

confidence: 71%

Section: Introductionmentioning

confidence: 97%

The Recent Evolution of a Symbiotic Ion Channel in the Legume Family Altered Ion Conductance and Improved Functionality in Calcium Signaling

et al. 2012

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“…Orthologs of DMI1 have been found; in Lotus japonicus, they are called CASTOR and POLLUX (Charpentier et al, 2008), and in pea (Pisum sativum), SYM8 . CASTOR and POLLUX, as well as calcium calmodulin-dependent protein kinase, are highly conserved both in legumes and nonlegumes (Banba et al, 2008;Chen et al, 2009). This highlights the essential role of the Ca 2+ oscillations in mycorrhizal signaling.…”

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confidence: 99%

Buffering Capacity Explains Signal Variation in Symbiotic Calcium Oscillations

et al. 2012

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Legumes form symbioses with rhizobial bacteria and arbuscular mycorrhizal fungi that aid plant nutrition. A critical component in the establishment of these symbioses is nuclear-localized calcium (Ca 2+ ) oscillations. Different components on the nuclear envelope have been identified as being required for the generation of the Ca 2+ oscillations. Among these an ion channel, Doesn't Make Infections1, is preferentially localized on the inner nuclear envelope and a Ca 2+ ATPase is localized on both the inner and outer nuclear envelopes. Doesn't Make Infections1 is conserved across plants and has a weak but broad similarity to bacterial potassium channels. A possible role for this cation channel could be hyperpolarization of the nuclear envelope to counterbalance the charge caused by the influx of Ca 2+ into the nucleus. Ca 2+ channels and Ca 2+ pumps are needed for the release and reuptake of Ca 2+ from the internal store, which is hypothesized to be the nuclear envelope lumen and endoplasmic reticulum, but the release mechanism of Ca 2+ remains to be identified and characterized. Here, we develop a mathematical model based on these components to describe the observed symbiotic Ca 2+ oscillations. This model can recapitulate Ca 2+ oscillations, and with the inclusion of Ca 2+ -binding proteins it offers a simple explanation for several previously unexplained phenomena. These include long periods of frequency variation, changes in spike shape, and the initiation and termination of oscillations. The model also predicts that an increase in buffering capacity in the nucleoplasm would cause a period of rapid oscillations. This phenomenon was observed experimentally by adding more of the inducing signal.

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“…All these rice mutants have been shown to be impaired in mycorrhizal symbiosis. [17][18][19][20] Of the 3 common Sym genes (for review see the ref.…”

Section: Are Common Symbiosis Genes Required For Endophytic Rice-rhizmentioning

confidence: 99%

“…All these rice mutants have been shown to be impaired in mycorrhizal symbiosis. [17][18][19][20] Of the 3 common Sym genes (for review see the ref. 2), Os-CASTOR encodes a nuclear-localized potassium channel protein; Os-DMI3 codes for a Ca 2+ /calmodulindependent protein kinase (CCaMK); and Os-CYCLOPS encodes a protein that interacts with and phophosphorylated by DMI3.…”

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confidence: 99%

Are common symbiosis genes required for endophytic rice-rhizobial interactions?

Chen

Zhu²

2013

Plant Signaling & Behavior

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The nitrogen-fixing bacteria, called rhizobia, are able to infect the roots of leguminous plants and induce the formation of root nodules. Within the root nodule, the bacteria can convert atmospheric nitrogen into ammonia, a biological form that can be directly used by the plant. Over the past decade, tremendous progress has been made in our understanding of the nodulation signaling pathway in legumes.1 It has become increasingly evident that the root nodule symbiosis has co-opted the signaling pathway that mediates the ancestral mycorrhizal symbiosis, a widespread mutualistic association between mycorrhizal fungi and the vast majority of land plants. [1][2][3][4][5] As such, most, if not all, legume genes required for root nodule symbiosis are already present in non-legumes, and these non-legume genes have been shown to function similarly to their legume counterparts. 2,6 These discoveries have reignited an old dream of plant biologists, i.e., to transfer the nitrogen-fixing symbiosis to cereals and other non-leguminous crops. 4,7 Despite being unable to induce nodulation, rhizobia have been shown to be able to infect and colonize the roots of nonlegumes such as rice (Oryza sativa). [8][9][10] This so-called "endophytic" interaction also can promote plant growth, even though the exact mechanisms for such positive responses are not well understood.9,11 Characterization of the infection and colonization processes of the rice-rhizobial association revealed that the bacteria primarily enter the plant tissue through root hairs and/ or crack entry located near the sites of newly emerging lateral roots.10 Similar infection strategies are also used by the rhizobia to enter the roots of the non-legume Paraponia and the water-tolerant legume Sesbania rostrata, both of which can nodulate with rhizobia.12-16 Intriguingly, similar to what occur in legumes, both root hair curling and infection thread-like structures were also Legume plants are able to establish root nodule symbioses with nitrogen-fixing bacteria, called rhizobia. recent studies revealed that the root nodule symbiosis has co-opted the signaling pathway that mediates the ancestral mycorrhizal symbiosis that occurs in most land plants. Despite being unable to induce nodulation, rhizobia have been shown to be able to infect and colonize the roots of non-legumes such as rice. one fascinating question is whether establishment of such associations requires the common symbiosis (Sym) genes that are essential for infection of plant cells by mycorrhizal fungi and rhizobia in legumes. here, we demonstrated that the common Sym genes are not required for endophytic colonization of rice roots by nitrogen-fixing rhizobia. Are common symbiosis genes required for endophytic rice-rhizobial interactions?Caiyan Chen 1 and hongyan Zhu Keywords: rice, rhizobia, nitrogen fixation, legume, common symbiosis genes observed on the rice roots inoculated with rhizobia. 10 However, in contrast to the root nodule symbiosis, in which bacteria colonize intracellularly, bacteria mainly resid...

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Antiquity and Function ofCASTORandPOLLUX, the Twin Ion Channel-Encoding Genes Key to the Evolution of Root Symbioses in Plants

Cited by 65 publications

References 94 publications

The Recent Evolution of a Symbiotic Ion Channel in the Legume Family Altered Ion Conductance and Improved Functionality in Calcium Signaling

The Recent Evolution of a Symbiotic Ion Channel in the Legume Family Altered Ion Conductance and Improved Functionality in Calcium Signaling

Buffering Capacity Explains Signal Variation in Symbiotic Calcium Oscillations

Are common symbiosis genes required for endophytic rice-rhizobial interactions?

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