Microtubule Dynamics in Living Root Hairs: Transient Slowing by Lipochitin Oligosaccharide Nodulation Signals

Vassileva, Valya; Kouchi, Hiroshi; Ridge, Robert W.

doi:10.1105/tpc.105.031641

Cited by 51 publications

(37 citation statements)

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“…The cytoskeletal changes that occur during tip growth of polarized root hairs 45 and the early effects of Nod factor on the root hair cytoskeleton that lead to root hair deformation have been subject to detailed analysis 13,46,47 . However, the cytoskeletal reorganizations involved in infection thread formation have not yet been thoroughly dissected.…”

Section: Sinorhizobium Meliloti Succinoglycan Biosynthesismentioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).The recent completion of the Sinorhizobium meliloti genome sequence, and the progress towards the completion of the Medicago truncatula genome sequence, have led to a surge in the molecular characterization of the determinants that are involved in the development of the symbiosis between rhizobial bacteria and leguminous plants. Aromatic compounds from legumes called flavonoids first signal the rhizobial bacteria to produce lipochitooligosaccharide compounds called Nod factors 1 . Nod factors that are secreted by the bacteria activate multiple responses in the host plant that prepare the plant to receive the invading bacteria. Nod factors and symbiotic exopolysaccharides induce the plant to form infection threads, which are thin tubules filled with bacteria that penetrate into the plant cortical tissue and deliver the bacteria to their target cells. Plant cells in the inner cortex internalize the invading bacteria in host-membrane-bound compartments that mature into structures known Correspondence to G.C.W. gwalker@mit.edu. Competing interests statementThe authors declare no competing financial interests. DATABASES Invasion of plant rootsAlthough plant roots are exposed to various micro-organisms in the soil, their cell walls form a strong protective barrier against most harmful species. The early steps in the invasion of barrel medic (M. truncatula) and alfalfa (Medicago sativa) roots by S. meliloti are characterized by the reciprocal exchange of signals that allow the bacteria to use the plant root hair cells as a means of entry. Initial signal exchangeFlavonoid compounds (2-phenyl-1,4-benzopyrone derivatives) produced by leguminous plants are the first signals to be exchanged by host-rhizobial symbiont pairs 1 (FIG. 1). Flavonoids bind bacterial NodD proteins, which are members of the LysR family of transcriptional regulators, and activate these proteins to induce the transcription of rhizobial genes 1,2 . For example, the M. sativa-derived flavonoid luteolin stimulates binding of an active form of NodD1 to an S. meliloti 'nod-box' p...

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Section: Sinorhizobium Meliloti Succinoglycan Biosynthesismentioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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“…Similarly, significant changes in the dynamic behavior of cortical and endoplasmic microtubules preceding nodule development and root hair curling were reported. These were found to be associated with all early steps during symbiotic interaction, including preinfection thread formation, initiation and polar growth of ITs, as well as the activation of root pericycle and cortical cells that initiates nodule primordia organogenesis (van Spronsen et al, 1995;Timmers et al, 1999;Vassileva et al, 2005). Given a well-recognized role of the cytoskeleton in mediating cell divisions and cell growth, including directionality and rate of cell expansion (Bannigan and Baskin, 2005), it was proposed that the observed Nod factordependent reorganization of microtubules and actin filaments might be a prerequisite for successful symbiotic interaction (van Spronsen et al, 1995;Timmers et al, 1999;Vassileva et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…In fact, one of the first cellular changes observed in root hairs responding to rhizobial inoculation or Nod factor application is an alteration in actin and microtubule organization (Cá rdenas et al, 1998;de Ruijter et al, 1999;Weerasinghe et al, 2003Weerasinghe et al, , 2005Vassileva et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Rearrangement of Actin Cytoskeleton Mediates Invasion ofLotus japonicusRoots byMesorhizobium loti

et al. 2009

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Infection thread-dependent invasion of legume roots by rhizobia leads to internalization of bacteria into the plant cells, which is one of the salient features of root nodule symbiosis. We found that two genes, Nap1 (for Nck-associated protein 1) and Pir1 (for 121F-specific p53 inducible RNA), involved in actin rearrangements were essential for infection thread formation and colonization of Lotus japonicus roots by its natural microsymbiont, Mesorhizobium loti. nap1 and pir1 mutants developed an excess of uncolonized nodule primordia, indicating that these two genes were not essential for the initiation of nodule organogenesis per se. However, both the formation and subsequent progression of infection threads into the root cortex were significantly impaired in these mutants. We demonstrate that these infection defects were due to disturbed actin cytoskeleton organization. Short root hairs of the mutants had mostly transverse or web-like actin filaments, while bundles of actin filaments in wild-type root hairs were predominantly longitudinal. Corroborating these observations, temporal and spatial differences in actin filament organization between wild-type and mutant root hairs were also observed after Nod factor treatment, while calcium influx and spiking appeared unperturbed. Together with various effects on plant growth and seed formation, the nap1 and pir1 alleles also conferred a characteristic distorted trichome phenotype, suggesting a more general role for Nap1 and Pir1 in processes establishing cell polarity or polar growth in L. japonicus.

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“…Root hair curling (Hac), continuous r growth that shifts inward toward the root hair shank, occurs in order to entrap rhizobia (12). In a root hair cell, NF triggers early symbiotic responses, such as depolarization of the plasma membrane, ion influx at the apex of the cell followed by an increase in the cytosolic Ca 2+ concentration at the tip of the root hair, a rhythmic Ca 2+ oscillation called Ca 2+ spiking, and rapid rearrangements of the actin cytoskeleton and microtubule structure within an hour (3,8,9,11,26,39,40). All these phenomena contribute to the distorted shape.…”

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confidence: 99%

Root Hair Deformation of Symbiosis-Deficient Mutants of Lotus japonicus by Application of Nod Factor from Mesorhizobium loti

Maekawa-Yoshikawa

Murooka

2009

Microb. Environ.

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In the model leguminous plant Lotus japonicus, the reception of a symbiotic signal called Nod factor (NF), which is secreted by the symbiont bacterium Mesorhizobium loti, induces wavy shaped root hairs. This is called root hair deformation. To dissect the root hair deformation process, we studied symbiosis-deficient mutants of L. japonicus, castor, nup85, ccamk and nsp2. The CASTOR, NUP85, and CCaMK genes are also required for mycorrhizal infection and thus called common symbiotic genes. On the global application of NF, all the mutants except nsp2 exhibited extensive branching of root hairs. The actin cytoskeleton was also observed as a marker for NF-dependent responses in mutant root hairs. At 2 hours of NF treatment, the ccamk mutant showed exaggerated swelling compared with the other mutants, indicating CCaMK to be required to terminate the swelling. In the nsp2 mutant, two hours of NF treatment remarkably induced swelling at root hair tips, although root hair deformation was not apparent at 24 hours of NF treatment. These results showed that common symbiotic components are involved in root hair deformation, which is regulated by a fine tuning mechanism early in the symbiosis between leguminous plants and rhizobia.

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Microtubule Dynamics in Living Root Hairs: Transient Slowing by Lipochitin Oligosaccharide Nodulation Signals

Cited by 51 publications

References 49 publications

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

Rearrangement of Actin Cytoskeleton Mediates Invasion ofLotus japonicusRoots byMesorhizobium loti

Root Hair Deformation of Symbiosis-Deficient Mutants of Lotus japonicus by Application of Nod Factor from Mesorhizobium loti

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