The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

Stührwohldt, Nils; Scholl, Stefan; Lang, Lisa; Katzenberger, Julia; Schumacher, Karin; Schaller, Andreas

doi:10.7554/elife.55580

Cited by 30 publications

(31 citation statements)

References 69 publications

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“…Cleavage of proPSK1 at D60 is fully consistent with our previous report on the biogenesis of CLEL6 and CLEL9. The respective precursors were found to be cleaved by SBT3.8 in an Asp-specific manner, and Asp was required in P1' for processing (Stührwohldt et al, 2020). Likewise, we show here that cleavage of Root Growth Factor (RGF1, alias CLEL8) by SBT3.8 depends on D104 (Supplementary Figure S1).…”

Section: Psk Precursor Processingsupporting

confidence: 65%

“….8 was expressed with a C-terminal hexa-His tag in tobacco (Nicotiana benthamiana) leaves and purified from cell wall extracts by affinity chromatography as described (Stührwohldt et al, 2020). C-terminally hexa-His-tagged proPSK1 was expressed in E. coli and purified by affinity chromatography, ultrafiltration, and size exclusion chromatography ( Figure 4B).…”

Section: Sbt3mentioning

confidence: 99%

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Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis

Stührwohldt

Bühler

Sauter

et al. 2020

Preprint

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Increasing drought stress poses a severe threat to agricultural productivity. Plants, however, evolved numerous mechanisms to cope with such environmental stress. Here we report that the stress-induced production of a peptide signal contributes to stress tolerance. The expression of phytosulfokine (PSK) peptide precursor genes, and transcripts of three subtilisin-like serine proteases, SBT1.4, SBT3.7 and SBT3.8 were found to be up-regulated in response to osmotic stress. Stress symptoms were enhanced in sbt3.8 loss-of-function mutants and could be alleviated by PSK treatment. Osmotic stress tolerance was improved in plants overexpression the precursor of PSK1 (proPSK1) or SBT3.8 resulting in higher fresh weight and improved lateral root development in the transgenic compared to wild-type plants. We further showed that SBT3.8 is involved in the biogenesis of the bioactive PSK peptide. ProPSK1 was cleaved by SBT3.8 at the C-terminus of the PSK pentapeptide. Processing by SBT3.8 depended on the aspartic acid residue adjacent to the cleavage site. ProPSK1 processing was impaired in the sbt3.8 mutant. The data suggest that increased expression in response to osmotic stress followed by the post-translational processing of proPSK1 by SBT3.8 leads to the production of PSK as a peptide signal for stress mitigation.

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Section: Psk Precursor Processingsupporting

confidence: 65%

Section: Sbt3mentioning

confidence: 99%

Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis

Stührwohldt

Bühler

Sauter

et al. 2020

Preprint

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“…EPI1 inhibits P69B, an abundant defense-induced SBT in the tomato apoplast (29). EPI1 also inhibits other SBTs and has been used to overcome functional redundancy of the SBT family in regulating floral organ abscission and the maturation of CLEL signaling peptides in Arabidopsis (30,31) and haustorium development in the parasitic plant Phtheirospermum japonicum (32). Preincubation of tomato AF with purified EPI1 prevented FP-TAMRA labeling of the 70-kDa SBTs but not of the 55-kDa SCPLs (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To test whether P69B is the protease that activates Rcr3 in tomato, we generated two independent transgenic antisense P69B (asP69B) tomato lines (16-32 and 16-34) ( 16 – 34 ) in the Money Maker (MM-Cf0) background. Since both lines behaved similarly in our assays, only 16-32 is shown as representative.…”

Section: Resultsmentioning

confidence: 99%

“…The use of EPI1 to block many unrelated SBTs simultaneously has been instrumental in our research and other investigations. EPI1 also has been used to overcome the redundancy of SBTs processing precursors of IDA and CLEL peptides, with regulate organ abscission and gravitropic responses in Arabidopsis (30,31), and SBTs involved in haustorium development in the parasitic plant P. japonicum (32). Future research strategies will benefit from the use of protease inhibitors like EPI1 in this "effector genetics" strategy.…”

mentioning

confidence: 99%

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Extracellular proteolytic cascade in tomato activates immune protease Rcr3

Paulus

Kourelis

Ramasubramanian

et al. 2020

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

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Proteolytic cascades regulate immunity and development in animals, but these cascades in plants have not yet been reported. Here we report that the extracellular immune protease Rcr3 of tomato is activated by P69B and other subtilases (SBTs), revealing a proteolytic cascade regulating extracellular immunity in solanaceous plants. Rcr3 is a secreted papain-like Cys protease (PLCP) of tomato that acts both in basal resistance against late blight disease (Phytophthora infestans) and in gene-for-gene resistance against the fungal pathogen Cladosporium fulvum (syn. Passalora fulva). Despite the prevalent model that Rcr3-like proteases can activate themselves at low pH, we found that catalytically inactive proRcr3 mutant precursors are still processed into mature mRcr3 isoforms. ProRcr3 is processed by secreted P69B and other Asp-selective SBTs in solanaceous plants, providing robust immunity through SBT redundancy. The apoplastic effector EPI1 of P. infestans can block Rcr3 activation by inhibiting SBTs, suggesting that this effector promotes virulence indirectly by preventing the activation of Rcr3(-like) immune proteases. Rcr3 activation in Nicotiana benthamiana requires a SBT from a different subfamily, indicating that extracellular proteolytic cascades have evolved convergently in solanaceous plants or are very ancient in the plant kingdom. The frequent incidence of Asp residues in the cleavage region of Rcr3-like proteases in solanaceous plants indicates that activation of immune proteases by SBTs is a general mechanism, illuminating a proteolytic cascade that provides robust apoplastic immunity.

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Small Post‐Translationally Modified Peptides – The Making Off

Stührwohldt

2022

Annual Plant Reviews Online

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Peptide hormones are an emerging new class of signalling molecules in plants, the importance of which has long been underestimated. One important class of peptides is the ‘small post‐translationally modified peptides’ (SPMPs), which require proteolytic processing as an essential step for maturation. SPMPs are derived from pre‐pro‐proteins that consist of 70 to 110 amino acids and harbour the mature peptides at, or close to their C‐termini. All SPMPs are subject to further post‐translational modifications during passage through the secretory pathway, including tyrosine sulphation and/or proline hydroxylation, which may be followed by O‐glycosylation. Despite the prevalence of hydroxyproline (Hyp) in SPMPs, the corresponding enzymes responsible for this post‐translational proline hydroxylation have not been identified, and it is unclear how the specificity of the proline targeted for hydroxylation is achieved. In this article, the current knowledge about the processing, biogenesis, compartmentalization, and post‐translational modifications of SPMPs will be discussed and analysed, and the open questions about the biogenesis of SPMPs will be pointed out.

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The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

Cited by 30 publications

References 69 publications

Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis

Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis

Extracellular proteolytic cascade in tomato activates immune protease Rcr3

Small Post‐Translationally Modified Peptides – The Making Off

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