A Nonsymbiotic Root Hair Tip Growth Phenotype in <i>NORK</i>-Mutated Legumes: Implications for Nodulation Factor–Induced Signaling and Formation of a Multifaceted Root Hair Pocket for Bacteria

Esseling, J.J.; Lhuissier, F.; Emons, A.M.C.

doi:10.1105/tpc.019653

Cited by 91 publications

(65 citation statements)

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“…Expression of a constitutively active allele of DMI3 induces these cell divisions and transcriptional changes, but does not induce root hair curling nor promote entry of bacteria, suggesting that these responses require other intermediates 24 . DMI2 encodes a leucine-rich-repeat receptor kinase that is required for tight root hair curling around the bacteria 25 . Two GRAS family transcriptional regulators, nodulation signalling pathway 1 (NSP1) and NSP2, are also required for Nod-factor-induced transcriptional changes 26,27 .…”

Section: Initial Signal Exchangementioning

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: Initial Signal Exchangementioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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“…Changes in the cytoskeleton, such as actin remodeling, occur within a few minutes after Nod factor application (Cá rdenas et al, 1998;Esseling et al, 2003Esseling et al, , 2004, triggering the activation of two different signal transduction pathways in the epidermal cells. One of them is linked to the expression of nodulins, and the other one is associated with root hair deformation through the modulation of components that normally are part of the machinery of the root hair growth.…”

Section: Root Hair Responses After Rhizobial Infectionmentioning

confidence: 99%

A Small GTPase of the Rab Family Is Required for Root Hair Formation and Preinfection Stages of the Common Bean–RhizobiumSymbiotic Association

et al. 2009

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Legume plants are able to establish a symbiotic relationship with soil bacteria from the genus Rhizobium, leading to the formation of nitrogen-fixing root nodules. Successful nodulation requires both the formation of infection threads (ITs) in the root epidermis and the activation of cell division in the cortex to form the nodule primordium. This study describes the characterization of RabA2, a common bean (Phaseolus vulgaris) cDNA previously isolated as differentially expressed in root hairs infected with Rhizobium etli, which encodes a protein highly similar to small GTPases of the RabA2 subfamily. This gene is expressed in roots, particularly in root hairs, where the protein was found to be associated with vesicles that move along the cell. The role of this gene during nodulation has been studied in common bean transgenic roots using a reverse genetic approach. Examination of root morphology in RabA2 RNA interference (RNAi) plants revealed that the number and length of the root hairs were severely reduced in these plants. Upon inoculation with R. etli, nodulation was completely impaired and no induction of early nodulation genes (ENODs), such as ERN1, ENOD40, and Hap5, was detected in silenced hairy roots. Moreover, RabA2 RNAi plants failed to induce root hair deformation and to initiate ITs, indicating that morphological changes that precede bacterial infection are compromised in these plants. We propose that RabA2 acts in polar growth of root hairs and is required for reorientation of the root hair growth axis during bacterial infection.

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“…Therefore, LYK3 is thought to mediate bacterial entry into root hairs (Catoira et al, 2001;Limpens et al, 2003;Smit et al, 2007). Downstream components of the NF signal transduction pathway in M. truncatula include DMI2, a leucine-rich repeat receptor kinase (Esseling et al, 2004), DMI1, a potassium ion channel (Ané et al, 2004;Riely et al, 2007), NENA, a nuclear pore component (Groth et al, 2010), CCaMK/DMI3, a Ca 2+ and calmodulin-dependent protein kinase (Lévy et al, 2004;Mitra et al, 2004), the CCaMK-regulated transcriptional regulator CY-CLOPS/IPD3 (Messinese et al, 2007;Yano et al, 2008;Singh et al, 2014), and various transcriptional regulators such as NSP1, NSP2, ERN1, and NIN (Kaló et al, 2005;Smit et al, 2005;Marsh et al, 2007, Middleton et al, 2007. As a consequence of NF signaling, the expression of many symbiotic genes such as the early nodulin gene ENOD11 is induced (Andriankaja et al, 2007;Hirsch et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Lei

Wang

et al. 2015

Plant Cell

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Rhizobia preferentially enter legume root hairs via infection threads, after which root hairs undergo tip swelling, branching, and curling. However, the mechanisms underlying such root hair deformation are poorly understood. Here, we showed that a type II small GTPase, ROP10, of Medicago truncatula is localized at the plasma membrane (PM) of root hair tips to regulate root hair tip growth. Overexpression of ROP10 and a constitutively active mutant (ROP10CA) generated depolarized growth of root hairs, whereas a dominant negative mutant (ROP10DN) inhibited root hair elongation. Inoculated with Sinorhizobium meliloti, the depolarized swollen and ballooning root hairs exhibited extensive root hair deformation and aberrant infection symptoms. Upon treatment with rhizobia-secreted nodulation factors (NFs), ROP10 was transiently upregulated in root hairs, and ROP10 fused to green fluorescent protein was ectopically localized at the PM of NF-induced outgrowths and curls around rhizobia. ROP10 interacted with the kinase domain of the NF receptor NFP in a GTP-dependent manner. Moreover, NF-induced expression of the early nodulin gene ENOD11 was enhanced by the overexpression of ROP10 and ROP10CA. These data suggest that NFs spatiotemporally regulate ROP10 localization and activity at the PM of root hair tips and that interactions between ROP10 and NF receptors are required for root hair deformation and continuous curling during rhizobial infection.

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A Nonsymbiotic Root Hair Tip Growth Phenotype in NORK-Mutated Legumes: Implications for Nodulation Factor–Induced Signaling and Formation of a Multifaceted Root Hair Pocket for Bacteria

Cited by 91 publications

References 60 publications

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

A Small GTPase of the Rab Family Is Required for Root Hair Formation and Preinfection Stages of the Common Bean–RhizobiumSymbiotic Association

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

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