BRASSINOSTEROID-SIGNALING KINASE1 Phosphorylates MAPKKK5 to Regulate Immunity in Arabidopsis

Yan, Haojie; Zhao, Yaofei; Shi, Hua; Li, Juan; Wang, Yingchun; Tang, Dingzhong

doi:10.1104/pp.17.01757

Cited by 111 publications

(106 citation statements)

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“…This includes the well-known defense regulator MPK3 (21) and previously discovered BIK1 (22). Another pathway found to be targeted is brassinosteroid (BR) signaling, with targets BRI1 (23), MAPKKK5 (24), PICKLE (25). BR has a clear role in defense, with connections to both BIK1 and MPK3 (26).…”

mentioning

confidence: 99%

Compensatory sequence variation between trans-species small RNAs and their target sites

Johnson

dePamphilis

Axtell

2019

Preprint

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Trans-species small regulatory RNAs (sRNAs) are delivered to host plants from diverse pathogens and parasites and can target host mRNAs. How trans-species sRNAs can be 10 effective on diverse hosts has been unclear. Multiple species of the parasitic plant Cuscuta produce trans-species sRNAs that collectively target many host mRNAs. Confirmed target sites are nearly always in highly conserved, protein-coding regions of host mRNAs. Cuscuta transspecies sRNAs can be grouped into superfamilies that have variation in a three-nucleotide period. These variants compensate for synonymous-site variation in host mRNAs. By targeting 15 host mRNAs at highly conserved protein-coding sites, and simultaneously expressing multiple variants to cover synonymous-site variation, Cuscuta trans-species sRNAs may be able to successfully target homologous mRNAs from diverse hosts. One Sentence Summary:The parasitic plant Cuscuta produces a diverse set of sRNAs that compensate for sequence variation in mRNA targets in diverse hosts. 20

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mentioning

confidence: 99%

Compensatory sequence variation between trans-species small RNAs and their target sites

Johnson

dePamphilis

Axtell

2019

Preprint

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“…Subsequent studies in Arabidopsis showed that both bsk1-1 and mapkkk5 mutants were more susceptible to DC3000 strains expressing AvrRpt2 or AvrRphB which are recognized by the CC-NLRs RPS2 and RPS5, respectively (39,40). However, the bsk1-1 and mapkkk5 mutants were similarly more susceptible to virulent DC3000, so the specific connection to NTI was unclear.…”

Section: Discussionmentioning

confidence: 99%

“…In Arabidopsis, AtBSK1 is a substrate of the BRI1 receptor kinase which initiates the brassinosteroid signaling pathway; this pathway has been completely defined and does not involve a M3K (63). Arabidopsis plants with loss-of-function mutations in BSK1 and rice plants with reduced expression of BSK1-2 do not have pronounced growth defects, although leaves of the Arabidopsis bsk1-1 mutant are slightly narrower than in wildtype plants and an AtBSK1 genomic clone can complement this phenotype (39,40,42). We have observed that N. benthamiana plants silenced with the SlMai1-1 and SlMai1-2 VIGS constructs are slightly smaller than unsilenced control plants and have longer, broader leaves.…”

Section: Discussionmentioning

confidence: 99%

“…BSK proteins lack key amino acids that are required for kinase activity, and thus have been predicted to be pseudokinases with putative roles as scaffold proteins (42)(43)(44). Although AtBSK1 also lacks these motifs, three papers, report that AtBSK1 autophosphorylates and can transphosphorylate AtMAPKKK5, and that the ATP binding site was required for its role in resistance to a fungal pathogen and PTI (39,40,45). We attempted to reproduce the kinase activity reported for AtBSK1 but were unable to see activity under our kinase assay conditions or those used for AtBSK1 (45) (Fig.…”

Section: Discussionmentioning

confidence: 99%

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Mai1 protein acts between host recognition of pathogen effectors and MAPK signaling

Hind

Roberts

Pedley

et al. 2019

Preprint

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The molecular mechanisms acting between host recognition of pathogen effectors by NOD-like receptor (NLR) proteins and mitogen-activated protein kinase (MAPK) signaling cascades are unknown. MAPKKK (M3K) activates MAPK signaling leading to programmed cell death (PCD) associated with NLR-triggered immunity. We identified a tomato M3K-interacting protein, SlMai1, that has 80% amino acid identity with Arabidopsis brassinosteroid kinase 1 (AtBsk1). SlMai1 has a protein kinase domain and a C-terminal tetratricopeptide repeat domain which interacts with the kinase domain of M3K. Virus-induced gene silencing of Mai1 homologs in Nicotiana benthamiana increased susceptibility to Pseudomonas syringae and compromised PCD induced by four NLR proteins. PCD was restored by expression of a synthetic SlMai1 gene that resists silencing. Expression of AtBsk1 did not restore PCD in Mai1-silenced plants, suggesting SlMai1 is functionally divergent from AtBsk1. PCD caused by overexpression of M3K or MKK2 was unaffected by Mai1 silencing indicating Mai1 acts upstream of these proteins. Co-expression of Mai1 with M3K in leaves enhanced MAPK phosphorylation and accelerated PCD. These findings reveal Mai1 as a molecular link acting between host recognition of pathogens and MAPK signaling. Author SummaryPlants use intracellular immune receptors to detect and respond to specific effector proteins which pathogens translocate into the host cell as part of their infection process. Localized programmed cell death (PCD) involving a mitogen-activated protein kinase (MAPK) cascade is an important host response associated with effector-triggered immunity, although the molecular connections between immune receptors and MAPK signaling is unknown. The Mai1 protein was found to act downstream of multiple immune receptors in Nicotiana benthamiana and to physically interact with MAPKKKα. The Mai1-MAPKKKα interaction enhances MAPK phosphorylation, triggers PCD and promotes disease resistance.Host responses activated by Pto/Prf are typical of NTI and include phosphorylation of mitogenassociated protein kinases (MAPKs) (23, 24), transcriptional reprogramming (22), and localized programmed cell death (PCD) (20, 25), which is thought to inhibit spread of the pathogen in host tissues.The role and mechanisms associated with MAPK signaling have been well-characterized in the Pto/Prf pathway. Virus-induced gene silencing (VIGS) of two tomato MAPKK genes (SlMKK1 and SlMKK2) and two MAPK genes (SlMPK2 or SlMPK3) compromised Pto/Prf-mediated resistance and initially revealed a role for MAPK cascades in this pathway (26, 27). NTI-associated MAPK signaling is also important in Arabidopsis and rice (24,(28)(29)(30)(31). A subsequent VIGS screen in N. benthamiana, which tested the effect of silencing >2400 randomly-chosen cDNAs on NTI, identified one MAPKKK, M3K, as playing an important role in Pto/Prf-mediated immunity (32). Silencing of M3K abolished PCD associated with Pto/Prf activation and also cell death associated with Pst-related disease symptoms (32). ...

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“…Despite distinct signaling outcomes, an accelerating number of RLKs and RLCKs are found to be shared by both BR and immune signaling pathways, such as BAK1 Chinchilla et al, 2007;Heese et al, 2007), BIR3 (Imkampe et al, 2017), and BSK1 (Tang et al, 2008;Shi et al, 2013;Yan et al, 2018). Recently, it was found that a positive regulator in plant immunity, BIK1, acts as a negative regulator in BR signaling by associating with BRI1.…”

Section: Researchmentioning

confidence: 99%

Identification of critical cysteine sites in brassinosteroid‐insensitive 1 and novel signaling regulators using a transient expression system

et al. 2019

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Summary The plant hormones brassinosteroids (BRs) modulate plant growth and development. Cysteine (Cys) residues located in the extracellular domain of a protein are of importance for protein structure by forming disulfide bonds. To date, the systematic study of the functional significance of Cys residues in BR‐insensitive 1 (BRI1) is still lacking. We used brassinolide‐induced exogenous bri1‐EMS‐Suppressor 1 (BES1) dephosphorylation in Arabidopsis thaliana protoplasts as a readout, took advantage of the dramatic decrease of BRI1 protein levels during protoplast isolation, and of the strong phosphorylation of BES1 by BR‐insensitive 2 (BIN2) in protoplasts, and developed a protoplast transient system to identify critical Cys sites in BRI1. Using this system, we identified a set of critical Cys sites in BRI1, as substitution of these Cys residues with alanine residues greatly compromised the function of BRI1. Moreover, we identified two negative regulators of BR signaling, pattern‐triggered immunity compromised RLCK1 (PCRK1) and PCRK2, that were previously known to positively regulate innate immunity signaling. This work not only provides insight into the functional importance of critical Cys residues in stabilizing the superhelical conformation of BRI1‐leucine‐rich‐repeat, but also reveals that PCRK1/2 can inversely modulate BR and plant immune signaling pathways.

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BRASSINOSTEROID-SIGNALING KINASE1 Phosphorylates MAPKKK5 to Regulate Immunity in Arabidopsis

Cited by 111 publications

References 51 publications

Compensatory sequence variation between trans-species small RNAs and their target sites

Compensatory sequence variation between trans-species small RNAs and their target sites

Mai1 protein acts between host recognition of pathogen effectors and MAPK signaling

Identification of critical cysteine sites in brassinosteroid‐insensitive 1 and novel signaling regulators using a transient expression system

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