RNA Splicing: A Novel Pathogen Effector Target

Abstract

Potato late blight caused by the notorious oomycete pathogen Phytophthora infestans led to the Irish famine in the 1840s. To date, this disease still remains a challenge for potato production (Figure 1). Effector proteins help P. infestans to infect their host plants, including potato and tomato. In summer 2004, in the Joint Genome Institute (Walnut Creek, California), some Phytophthora researchers gathered at an “Effector table,” and by aligning the amino acid sequences of many unpublished effector proteins from Phytophthora pathogens, revealed that all of them possess conserved Arg-any residue-Leu-Arg (RXLR) and Glu-Glu-Arg (EER) motifs post signal peptides (Govers and Gijzen, 2006Govers F. Gijzen M. Phytophthora genomics: the plant destroyers' genome decoded.Mol. Plant Microbe Interact. 2006; 19: 1295-1301Crossref PubMed Scopus (50) Google Scholar). In 2009, the genome sequence of P. infestans strain T30-4 was published and 563 RXLR effectors were predicted. Since then, many high-throughput "effectoromics" screening strategies were carried out and effectors were identified that trigger a hypersensitive response (HR) on some host genotypes, or that function as cell death repressors or RNA silencing suppressors. However, the function of most RXLR effectors remains unknown. A new study by Huang et al., 2020Huang J. Lu X. Wu H. Xie Y. Peng Q. Gu L. Wu J. Wang Y. Reddy A.S.N. Dong S. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity.Mol. Plant. 2020; (In this issue)https://doi.org/10.1016/j.molp.2020.07.007Abstract Full Text Full Text PDF Scopus (6) Google Scholar discovered that Phytophthora effectors can reprogram host immunity through modulating alternative splicing (AS) of host mRNAs in tomato. Plant immune systems operate in multiple layers, one of which involves AS that is known to play roles in both microbe-associated molecular pattern (MAMP)-triggered immunity and effector-triggered immunity. To gain insight into potential AS-regulated plant immunity during pathogen attack, Huang et al., 2020Huang J. Lu X. Wu H. Xie Y. Peng Q. Gu L. Wu J. Wang Y. Reddy A.S.N. Dong S. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity.Mol. Plant. 2020; (In this issue)https://doi.org/10.1016/j.molp.2020.07.007Abstract Full Text Full Text PDF Scopus (6) Google Scholar first investigated tomato transcriptome changes during P. infestans infection and identified 2088 alternatively spliced genes in response to pathogen infection. To investigate how P. infestans manipulates plant AS and to identify specific splicing regulatory effectors (SREs), they developed an alternative splicing reporter system, in which the alternatively spliced region of RLPK, a known protein kinase gene that undergoes AS upon pathogen attack, is fused with the luciferase (LUC) gene, and a stable 35S-RLPK-LUC transgenic Nicotiana benthamiana line was generated. The RLPK.1 transcript produces functional luciferase, but upon AS, the RLPK.2 carries a premature stop codon, preventing luciferase expression. Using this system, they tested 87 RXLR effectors from P. infestans and identified 9 SREs. Furthermore, they found that these SREs bind splicing factors to modulate plant AS. Specifically, SRE3 (Pi06094) can physically interact with a splicing factor U1-70k and promote virulence of P. infestans (Huang et al., 2020Huang J. Lu X. Wu H. Xie Y. Peng Q. Gu L. Wu J. Wang Y. Reddy A.S.N. Dong S. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity.Mol. Plant. 2020; (In this issue)https://doi.org/10.1016/j.molp.2020.07.007Abstract Full Text Full Text PDF Scopus (6) Google Scholar). The versatile reporter system for identifying AS-regulating effectors developed by Huang et al., 2020Huang J. Lu X. Wu H. Xie Y. Peng Q. Gu L. Wu J. Wang Y. Reddy A.S.N. Dong S. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity.Mol. Plant. 2020; (In this issue)https://doi.org/10.1016/j.molp.2020.07.007Abstract Full Text Full Text PDF Scopus (6) Google Scholar could be applied to effectors from other plant pathogens and will deepen our understanding of how AS manipulates plant immunity. It is noteworthy that one of the SREs (SRE4, PITG_07569) was recently reported as the Avr effector of a broad-spectrum R gene Rpi-amr1 from Solanum americanum (Lin et al., 2020Lin X. Song T. Fairhead S. et al.Identification of Avramr1 from Phytophthora infestans using long read and cDNA pathogen-enrichment sequencing (PenSeq).Mol. Plant Pathol. 2020; https://doi.org/10.1111/mpp.12987Crossref Scopus (4) Google Scholar). Investigating how these SREs interact with their host targets to modulate AS and how plant immune receptors can recognize them to activate host immunity might lead to new disease control strategies. No conflict of interest declared.