Involvement of papain and legumain proteinase in the senescence process of <i><scp>M</scp>edicago truncatula</i> nodules

Pierre, Olivier; Hopkins, Julie; Combier, Maud; Baldacci, Fabien; Engler, Gilbert; Brouquisse, Renaud; Hérouart, Didier; Boncompagni, Éric

doi:10.1111/nph.12717

Cited by 53 publications

(72 citation statements)

References 84 publications

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“…evaluated recently: MtCP6, which encodes a papain-like proteolytic enzyme, and MtVPE, which encodes a caspase-like enzyme (15). At 21 dpi, we find that these markers are induced in A20 plants inoculated with hrrP + rhizobia but not A17 plants inoculated with the same strain (Fig.…”

Section: Identification Of Host Range Restriction Peptidase As a Nitrmentioning

confidence: 56%

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Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility

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Dillon

et al. 2015

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

116

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Legume-rhizobium pairs are often observed that produce symbiotic root nodules but fail to fix nitrogen. Using the Sinorhizobium meliloti and Medicago truncatula symbiotic system, we previously described several naturally occurring accessory plasmids capable of disrupting the late stages of nodule development while enhancing bacterial proliferation within the nodule. We report here that host range restriction peptidase (hrrP), a gene found on one of these plasmids, is capable of conferring both these properties. hrrP encodes an M16A family metallopeptidase whose catalytic activity is required for these symbiotic effects. The ability of hrrP to suppress nitrogen fixation is conditioned upon the genotypes of both the host plant and the hrrPexpressing rhizobial strain, suggesting its involvement in symbiotic communication. Purified HrrP protein is capable of degrading a range of nodule-specific cysteine-rich (NCR) peptides encoded by M. truncatula. NCR peptides are crucial signals used by M. truncatula for inducing and maintaining rhizobial differentiation within nodules, as demonstrated in the accompanying article [Horváth B, et al. (2015) Proc Natl Acad Sci USA, 10.1073/pnas.1500777112]. The expression pattern of hrrP and its effects on rhizobial morphology are consistent with the NCR peptide cleavage model. This work points to a symbiotic dialogue involving a complex ensemble of host-derived signaling peptides and bacterial modifier enzymes capable of adjusting signal strength, sometimes with exploitative outcomes.symbiosis | nitrogen fixation | metallopeptidase | NCR peptides

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Section: Identification Of Host Range Restriction Peptidase As a Nitrmentioning

confidence: 56%

“…Total RNA was extracted from M. truncatula A17 and A20 nodules, and cDNA pools were synthesized using standard techniques. Quantitative real-time PCR (qRT-PCR) analyses for MtCP6 and MtVPE were performed as described by Pierre et al (15) using the constitutively expressed MtC27 and MtA39 genes as endogenous controls.…”

Section: Methodsmentioning

confidence: 99%

Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility

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Tanner

Dillon

et al. 2015

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

116

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“…Protease activity, expressed as Δ (fluorescence) min −1 , was measured as described by Pierre et al . ().…”

Section: Methodsmentioning

confidence: 97%

Drought‐induced senescence of Medicago truncatula nodules involves serpin and ferritin to control proteolytic activity and iron levels

et al. 2018

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Drought is a major constraint for legume growth and yield. Senescence of nitrogen-fixing nodules is one of the early drought responses and may cause nutrient stress in addition to water stress in legumes. For nodule senescence to function as part of a drought-survival strategy, we propose that the intrinsically destructive senescence process must be tightly regulated. Medicago truncatula protease inhibitor and iron scavenger-encoding genes, possibly involved in controlling nodule senescence, were identified. RNA interference (RNAi) lines were constructed in which expression of a serpin or ferritins was knocked down. Both wild-type and RNAi lines were subjected to drought stress and nodule activity and plant physiological responses were measured. Drought caused M. truncatula to initiate nodule senescence before plant growth was affected and before an increase in papain-like proteolytic activity and free iron levels was apparent. Knock-down expression of serpin6 and ferritins caused increased protease activity, free iron levels, early nodule senescence and reduced plant growth. The results suggest that M. truncatula nodule-expressed serpin6 and ferritins mediate ordered drought-induced senescence by regulating papain-like cysteine protease activity and free iron levels. This strategy may allow the drought-stressed plants to benefit maximally from residual nitrogen fixation and nutrient recovery resulting from break down of macromolecules.

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“…were characterized as genes involved in senescence and programmed cell death in response to infections (H atsugai et al 2004;Pierre et al 2014). These genes are also important for maintenance of the endoplasmic reticulum stress pathway, which induces vacuolar cell death, mediated by legumain/caspase-1-like activities during microbial colonization (Qiang et al 2012).…”

Section: Plant Materialsmentioning

confidence: 98%

“…Physiologically, proteolysis is extremely important for plant germination, growth, senescence, and defense pathways (van der Hoorn 2008). Several of these processes involve cysteine proteases that can be controlled by phytocystatin inhibition, including the degradation of storage proteins to provide a nutrient source for seedling development important to plant development, homeostasis, and defense responses (Dutt et al 2010;Lepelley et al 2012;Quain et al 2014;Pierre et al 2014). Until recently, the majority of studies only considered the roles of group I phytocystatins in relation to papain-like proteinases (C1A) (Abe et al 1988;Belenghi et al 2003;Ohtsubo et al 2005;Martinez et al 2005Martinez et al , 2009Hong et al 2007;Hwang et al 2009), leaving a knowledge gap regarding group II phytocystatins and their possible target proteases.…”

Section: Introductionmentioning

confidence: 99%

Rice bifunctional phytocystatin is a dual modulator of legumain and papain-like proteases

et al. 2016

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Phytocystatins are well-known inhibitors of C1A cysteine proteinases. However, previous research has revealed legumain (C13) protease inhibition via a carboxy-extended phytocystatin. Among the 12 phytocystatins genes in rice, OcXII is the only gene possessing this carboxy-terminal extension. The specific legumain inhibition activity was confirmed, in our work, using a recombinant OcXII harboring only the carboxy-terminal domain and this part did not exhibit any effect on papain-like activities. Meanwhile, rice plants silenced at the whole OcXII gene presented higher legumain and papain-like proteolytic activities, resulting in a faster initial seedling growth. However, when germinated under stressful alkaline conditions, OcXII-silenced plants exhibited impaired root formation and delayed shoot growth. Interestingly, the activity of OcXII promoter gene was detected in the rice seed scutellum region, and decreases with seedling growth. Seeds from these plants also exhibited slower growth at germination under ABA or alkaline conditions, while maintaining very high levels of OcXII transcriptional activation. This likely reinforces the proteolytic control necessary for seed germination and growth. In addition, increased legumain activity was detected in OcXII RNAi plants subjected to a fungal elicitor. Overall, the results of this study highlight the association of OcXII with not only plant development processes, but also with stress response pathways. The results of this study reinforce the bifunctional ability of carboxy-extended phytocystatins in regulating legumain proteases via its carboxy-extended domain and papain-like proteases by its amino-terminal domain.

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Involvement of papain and legumain proteinase in the senescence process of Medicago truncatula nodules

Cited by 53 publications

References 84 publications

Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility

Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility

Drought‐induced senescence of Medicago truncatula nodules involves serpin and ferritin to control proteolytic activity and iron levels

Rice bifunctional phytocystatin is a dual modulator of legumain and papain-like proteases

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