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Biology subjects

Chia, K.-S.

Publications and source records attributed to Chia, K.-S..

9 recordsLinked to original sources

A Blast Fungus Effector Targets a Tubby-like F-box Protein to Suppress Plant Immunity

The blast fungus Magnaporthe oryzae is one of the most destructive pathogens of rice, secreting effector proteins that reprogram host cells to enable infection. Identifying plant targets of these fungal effectors is central to understanding how blast disease is established, but the targets and mechanisms of most effectors remain unknown. Here, we show that a Zinc finger (ZiF)-family effector, Tie1, targets the rice Tubby-like protein (TLP) family, which are membrane-associated plant immunity regulators whose exact functions have not been defined. Tie1 binds a range of rice TLPs and specifically engages with the Tubby-like domain of OsTLP7. Co-expression in planta with Tie1 re-localises this domain from the plasma membrane to the cytoplasm and nucleus, a shift also observed by disrupting the OsTLP7 phosphatidylinositol 4,5-bisphosphate (PIP2)-binding site in the absence of the effector. By combining AlphaFold3 structural predictions with allelic variation, we define a putative Tie1/OsTLP7 interface distal to the PIP2-binding site. Furthermore, Tie1 induces transcriptional activation activity of the OsTLP7 Tubby-like domain, and Tie1 overexpression in stable Arabidopsis lines leads to upregulation of genes that repress jasmonic acid (JA) signalling. Taken together, our results indicate that Tie1 inhibits PIP2 binding by OsTLP7 to drive its re-localisation to the nucleus and thereby modulating transcription to suppress JA-mediated plant immunity.

plant biology↗

Canonical NLR immune receptor architecture enforces EDS1-dependency onto divergent TIR domains

Toll/interleukin-1 receptor (TIR) enzymes are prominent immune components in diverse organisms across the tree of life. In flowering plants, TIRs are often integrated into nucleotide binding leucine-rich repeat (NLR) receptors whose oligomerization-dependent biochemical activities create second messengers perceived by ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1)-family signaling complexes. TIR-NLRs and TIR proteins are present across the full spectrum of plant evolution, yet EDS1 signaling is a derived trait in seed plants. Here, we examined the functional dependency of diverse plant TIRs on the EDS1 pathway in the angiosperms Nicotiana benthamiana and Nicotiana tabacum. While the isolated TIR domains from non-seed plants generally required EDS1 for immune cell death activation, we also identified TIRs that functioned independent of EDS1. However, chimeric TIR-NLRs incorporating these diverse TIR domains onto the AtWRR4a receptor chassis showed a full reversion to EDS1-dependency. Extending this phenomenon further, we demonstrated that the AtWRR4a architecture enforces EDS1-dependence onto a bacterial TIR domain that is otherwise EDS1-independent. Collectively, our work demonstrates that NLR immune receptor architecture influences TIR-related immunity and provides further context to their ancient acquisition into plant immune systems.

plant biology↗

Herbaria provide a valuable resource for obtaining informative mRNA

While DNA has built the framework for molecular insights from museum collections, the utility of archival RNA remains largely unexplored. Likely a consequence of the known instability of RNA relative to DNA, this has effectively precluded the use of herbaria for transcriptomics. Here, we challenge the assumption that herbaria cannot be used for transcriptomics by assembling transcriptomes from RNA extracted from herbarium specimens. Through systematic comparison of transcriptomes from fresh-collected, silica-dried, and archival specimens, we demonstrate the suitability of herbarium-derived RNA for transcriptomics. We show the practical applicability of archival mRNA by functionally validating a plant immune receptor synthesized from a specimen collected in 1956. These results contradict the community consensus regarding archival RNA and open the door to subsequent transcriptomic explorations of rare and extinct plant species. Our findings highlight the importance of preserving and utilizing the diversity embedded within herbarium collections.

plant biology↗

Conserved effectors underpin the virulence of liverwort-isolated Pseudomonas in divergent plants

Plant pathogenic Pseudomonas species naturally antagonize a diverse range of flowering plants. While emerging research demonstrates that isolates belonging to the P. syringae species complex colonize diverse hosts, the extent to which these bacteria naturally infect non-flowering plants like the model liverwort Marchantia polymorpha remains unclear. Here, we identify natural associations between Pseudomonas viridiflava and the liverwort Marchantia polymorpha. Pseudomonas bacteria isolated from diseased liverworts in the wild successfully re-infected M. polymorpha in pure culture conditions, producing high in planta bacterial densities and causing prominent tissue maceration. Comparative genomic analysis of Marchantia-associated P. viridiflava identified core virulence machinery like the type-III secretion system (T3SS) and conserved effectors (AvrE and HopM1) that were essential for liverwort infection. Disease assays performed in Nicotiana benthamiana further confirmed that liverwort-associated P. viridiflava infect flowering plants in an effector-dependent manner. Our work highlights P. viridiflava as an effective broad host pathogen that relies on conserved virulence factors to manipulate evolutionarily divergent host plants.

plant biology↗

A Necrotizing Toxin Promotes Pseudomonas syringae Infection Across Evolutionarily Divergent Plant Lineages

The Pseudomonas syringae species complex harbors a diverse range of plant pathogenic bacteria. While much of the current understanding of P. syringae is centered on interactions with flowering plants, much less is known about infection in evolutionarily divergent non-flowering lineages. Here, we took a comparative evolutionary approach to understand how P. syringae infects distantly related plants. We identify broad host P. syringae isolates causing significant disease in the liverwort Marchantia polymorpha, the fern Ceratopteris richardii, and the flowering plant Nicotiana benthamiana, which last shared a common ancestor over 500 million years ago. We demonstrate that phytotoxin enriched isolates belonging to the phylogroup 2 clade of the P. syringae species complex are particularly virulent in non-flowering plants, relying on a combination of type-3 secreted effector proteins and the lipopeptide phytotoxin syringomycin. The application of purified syringomycin promotes necrosis in diverse host tissues and activates conserved genes associated with redox regulation and cell death. Toxin-deficient phylogroups normally unable to infect Marchantia thalli exhibit enhanced bacterial growth when supplemented with exogenous syringomycin, further highlighting its role as a host-range defining factor in Pseudomonas. Collectively our research reveals a key role for the lipopeptide syringomycin in promoting Pseudomonas colonization, which works in concert with type-3 effector proteins to antagonize an exceptionally wide spectrum of land plants.

plant biology↗

The N-terminal executioner domains of NLR immune receptors are functionally conserved across major plant lineages

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins are a prominent class of intracellular immune receptors that are present across diverse plant lineages. However, our understanding of plant NLR structure and function is limited to the evolutionarily young flowering plant clade (angiosperms). Here, we describe an extended spectrum of NLR diversity across major plant lineages and demonstrate functional conservation of N-terminal executioner domains that trigger immune responses. We show that broadly distributed CC (coiled-coil) and TIR (toll/interleukin-1 receptor) domains retain executioner function through trans-lineage activation of immune-related cell death in the model angiosperm Nicotiana benthamiana. Further examination of a CC subfamily specific to non-flowering lineages uncovered an essential N-terminal MAEPL motif with functional similarity to resistosome-forming CC-NLRs. Ectopic activation of the MAEPL-type CC in the divergent liverwort Marchantia polymorpha led to profound growth inhibition, defense gene activation, and signatures of cell death resembling CC activity in flowering plants. Moreover, comparative macroevolutionary transcriptomics in Marchantia and Nicotiana identified conserved CC responsive genes, providing further insight into the core aspects of CC function shared between flowering and non-flowering plants. Our findings highlight the need to understand NLR structure and function across the full spectrum of plant diversity.

plant biology↗

TOPLESS promotes plant immunity by repressing auxin signaling and is targeted by the fungal effector Naked1

In plants, the antagonism between growth and defense is hardwired by hormonal signaling. Perception of Pathogen Associated Molecular Patterns (PAMPs) from invading microorganisms inhibits auxin signaling and growth. Conversely, pathogens manipulate auxin signaling to promote disease, but how this hormone inhibits immunity is not fully understood. Ustilago maydis is a maize pathogen that induces auxin signaling in its host. We characterized an U. maydis effector protein, Naked1 (Nkd1), that is translocated into the host nucleus. Through its native EAR motif, Nkd1 binds to the transcriptional co-repressors TOPLESS/TOPLESS related (TPL/TPRs) and prevents the recruitment of transcriptional repressors involved in hormonal signaling, leading to de-repression of auxin and jasmonate signaling. Moderate up-regulation of auxin signaling inhibits an early defense response, PAMP-triggered ROS burst. Thus, our findings establish a clear mechanism for auxin-induced pathogen susceptibility. Manipulation of TPL by Nkd1 is evolutionary well balanced as engineered Nkd1 variants with increased expression or increased EAR-mediated TPL/TPR binding trigger typical salicylic acid mediated defense reactions, leading to pathogen resistance.

plant biology↗

A cross-kingdom conserved ER-phagy receptor maintains endoplasmic reticulum homeostasis during stress

Eukaryotes have evolved various quality control mechanisms to promote proteostasis in the ER. Selective removal of certain ER domains via autophagy (termed as ER-phagy) has emerged as a major quality control mechanism. However, the degree to which ER-phagy is employed by other branches of ER-quality control remains largely elusive. Here, we identify a cytosolic protein, C53, that is specifically recruited to autophagosomes during ER-stress, in both plant and mammalian cells. C53 interacts with ATG8 via a distinct binding epitope, featuring a shuffled ATG8 interacting motif (sAIM). C53 senses proteotoxic stress in the ER lumen by forming a tripartite receptor complex with the ER-associated ufmylation ligase UFL1 and its membrane adaptor DDRGK1. The C53/UFL1/DDRGK1 receptor complex is activated by stalled ribosomes and induces the degradation of internal or passenger proteins in the ER. Consistently, the C53 receptor complex and ufmylation mutants are highly susceptible to ER stress. Thus, C53 forms an ancient quality control pathway that bridges selective autophagy with ribosome-associated quality control at the ER.

cell biology↗

Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

Ustilago maydis (U. maydis) is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins which suppress immune responses and redirect the host-metabolism in favor of the pathogen. Here we describe a novel strategy by which U. maydis induces plant jasmonate/ethylene (JA/ET) hormone signaling and thereby biotrophic susceptibility. The U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1) possesses an ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motif, DLNxxP, which interacts with the second WD40 domain of the conserved plant co-repressor family Topless/Topless related (TPL/TPR). Jsi1 interaction with TPL/TPRs leads to derepression of the ethylene response factor (ERF) branch of the JA/ET signaling pathway, supporting biotrophic susceptibility. Jsi1 likely activates the ERF branch by interfering with the binding of endogenous DLNxxP motif-containing ERF transcription factors to TPL/TPR proteins. The identification of effector proteins possessing a DLNxxP motif in different fungal species with biotrophic and hemibiotrophic lifestyles together with the validation of the interaction between such effectors from Magnaporthe oryzae (M. oryzae), Sporisorium scitamineum (S. scitamineum), and S. reilianum with TPL proteins indicates the convergent evolution of effectors for modulating the TPL/TPR co-repressor hub.

plant biology↗