1932

Abstract

Alternative splicing (AS) is an evolutionarily conserved cellular process in eukaryotes in which multiple messenger RNA (mRNA) transcripts are produced from a single gene. The concept that AS adds to transcriptome complexity and proteome diversity introduces a new perspective for understanding how phytopathogen-induced alterations in host AS cause diseases. Recently, it has been recognized that AS represents an integral component of the plant immune system during parasitic, commensalistic, and symbiotic interactions. Here, I provide an overview of recent progress detailing the reprogramming of plant AS by phytopathogens and the functional implications on disease phenotypes. Additionally, I discuss the vital function of AS of immune receptors in regulating plant immunity and how phytopathogens use effector proteins to target key components of the splicing machinery and exploit alternatively spliced variants of immune regulators to negate defense responses. Finally, the functional association between AS and nonsense-mediated mRNA decay in the context of plant–pathogen interface is recapitulated.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-121423-041908
2024-09-09
2025-02-14
Loading full text...

Full text loading...

/deliver/fulltext/phyto/62/1/annurev-phyto-121423-041908.html?itemId=/content/journals/10.1146/annurev-phyto-121423-041908&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ayliffe MA, Frost DV, Finnegan EJ, Lawrence GJ, Anderson PA, Ellis JG. 1999.. Analysis of alternative transcripts of the flax L6 rust resistance gene. . Plant J. 17::28792
    [Crossref] [Google Scholar]
  2. 2.
    Balistreri G, Bognanni C, Mühlemann O. 2017.. Virus escape and manipulation of cellular nonsense-mediated mRNA decay. . Viruses 9::24
    [Crossref] [Google Scholar]
  3. 3.
    Barta A, Kalyna M, Reddy ASN. 2010.. Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. . Plant Cell 22::292629
    [Crossref] [Google Scholar]
  4. 4.
    Barta A, Marquez Y, Brown JWS. 2012.. Challenges in plant alternative splicing. . In Alternative Pre-mRNA Splicing: Theory and Protocols, ed. CWJ Smith, R Lührmann , pp. 7991. Weinheim, Ger.:: Wiley-VCH Verlag
    [Google Scholar]
  5. 5.
    Bedre R, Irigoyen S, Schaker PDC, Monteiro-Vitorello CB, Da Silva JA, Mandadi KK. 2019.. Genome-wide alternative splicing landscapes modulated by biotrophic sugarcane smut pathogen. . Sci. Rep. 9::8876
    [Crossref] [Google Scholar]
  6. 6.
    Betz R, Heidt S, Figueira-Galan D, Langner T, Requena N. 2023.. Alternative splicing regulation in plants by effectors of symbiotic arbuscular mycorrhizal fungi. . bioRxiv 558436. https://doi.org/10.1101/2023.09.20.558436
  7. 7.
    Bourcy M, Brocard L, Pislariu CI, Cosson V, Mergaert P, et al. 2013.. Medicago truncatula DNF2 is a PI-PLC-XD-containing protein required for bacteroid persistence and prevention of nodule early senescence and defense-like reactions. . New Phytol. 197::125061
    [Crossref] [Google Scholar]
  8. 8.
    Brogna S, Wen J. 2009.. Nonsense-mediated mRNA decay (NMD) mechanisms. . Nat. Struct. Mol. Biol. 16::10713
    [Crossref] [Google Scholar]
  9. 9.
    Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 2007.. A novel role for the TIR domain in association with pathogen-derived elicitors. . PLOS Biol. 5::e68
    [Crossref] [Google Scholar]
  10. 10.
    Campo S, Peris-Peris C, Siré C, Moreno AB, Donaire L, et al. 2013.. Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. . New Phytol. 199::21227
    [Crossref] [Google Scholar]
  11. 11.
    Chung HS, Cooke TF, DePew CL, Patel LC, Ogawa N, et al. 2010.. Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling. . Plant J. 63::61322
    [Crossref] [Google Scholar]
  12. 12.
    Dahale SK, Ghosh D, Ingole KD, Chugani A, Kim SH, Bhattacharjee S. 2021.. HopA1 effector from Pseudomonas syringae pv syringae strain 61 affects NMD processes and elicits effector-triggered immunity. . Int. J. Mol. Sci. 22::7440
    [Crossref] [Google Scholar]
  13. 13.
    De Palma M, Salzano M, Villano C, Aversano R, Lorito M, et al. 2019.. Transcriptome reprogramming, epigenetic modifications and alternative splicing orchestrate the tomato root response to the beneficial fungus Trichoderma harzianum. . Horticult. Res. 6::5
    [Crossref] [Google Scholar]
  14. 14.
    Delessert C, Kazan K, Wilson IW, Straeten DVD, Manners J, et al. 2005.. The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. . Plant J. 43::74557
    [Crossref] [Google Scholar]
  15. 15.
    Dinesh-Kumar SP, Baker BJ. 2000.. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. . PNAS 97::190813
    [Crossref] [Google Scholar]
  16. 16.
    Docquier S, Tillemans V, Deltour R, Motte P. 2004.. Nuclear bodies and compartmentalization of pre-mRNA splicing factors in higher plants. . Chromosoma 112::25566
    [Crossref] [Google Scholar]
  17. 17.
    Drechsel G, Kahles A, Kesarwani AK, Stauffer E, Behr J, et al. 2013.. Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome. . Plant Cell 25::372642
    [Crossref] [Google Scholar]
  18. 18.
    Dvinge H. 2018.. Regulation of alternative mRNA splicing: old players and new perspectives. . FEBS Lett. 592::29873006
    [Crossref] [Google Scholar]
  19. 19.
    Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, et al. 2010.. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. . Genome Res. 20::4558
    [Crossref] [Google Scholar]
  20. 20.
    Filichkin SA, Priest HD, Megraw M, Mockler TC. 2015.. Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress. . Curr. Opin. Plant Biol. 24::12535
    [Crossref] [Google Scholar]
  21. 21.
    Fluhr R. 2008.. Regulation of splicing by protein phosphorylation. . Curr. Top. Microbiol. Immunol. 326::11938
    [Google Scholar]
  22. 22.
    Fu ZQ, Guo M, Jeong B-R, Tian F, Elthon TE, et al. 2007.. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. . Nature 447::28488
    [Crossref] [Google Scholar]
  23. 23.
    Gallo MCR, Uhrig RG. 2023.. Phosphorylation mediated regulation of RNA splicing in plants. . Front. Plant Sci. 14::1249057
    [Crossref] [Google Scholar]
  24. 24.
    Gelfman S, Cohen N, Yearim A, Ast G. 2013.. DNA-methylation effect on cotranscriptional splicing is dependent on GC architecture of the exon–intron structure. . Genome Res. 23::78999
    [Crossref] [Google Scholar]
  25. 25.
    Gervasi F, Ferrante P, Dettori MT, Scortichini M, Verde I. 2018.. Transcriptome reprogramming of resistant and susceptible peach genotypes during Xanthomonas arboricola pv. pruni early leaf infection. . PLOS ONE 13::e0196590
    [Crossref] [Google Scholar]
  26. 26.
    Gloggnitzer J, Akimcheva S, Srinivasan A, Kusenda B, Riehs N, et al. 2014.. Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. . Cell Host Microbe 16::37690
    [Crossref] [Google Scholar]
  27. 27.
    Gui X, Zhang P, Wang D, Ding Z, Wu X, et al. 2022.. Phytophthora effector PSR1 hijacks the host pre-mRNA splicing machinery to modulate small RNA biogenesis and plant immunity. . Plant Cell 34::344359
    [Crossref] [Google Scholar]
  28. 28.
    Halterman DA, Wei F, Wise RP. 2003.. Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. . Plant Physiol. 131::55867
    [Crossref] [Google Scholar]
  29. 29.
    Halterman DA, Wise RP. 2006.. Upstream open reading frames of the barley Mla13 powdery mildew resistance gene function co-operatively to down-regulate translation. . Mol. Plant Pathol. 7::16776
    [Crossref] [Google Scholar]
  30. 30.
    Hawk TE, Piya S, Zadegan SB, Li P, Rice JH, Hewezi T. 2023.. The soybean immune receptor GmBIR1 regulates host transcriptome, spliceome, and immunity during cyst nematode infection. . New Phytol. 239::233552
    [Crossref] [Google Scholar]
  31. 31.
    Hewezi T, Juvale PS, Piya S, Maier TR, Rambani A, et al. 2015.. The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. . Plant Cell 27::891907
    [Crossref] [Google Scholar]
  32. 32.
    Hewezi T, Piya S, Qi M, Balasubramaniam M, Rice JH, Baum TJ. 2016.. Arabidopsis miR827 mediates post-transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. . Plant J. 88::17992
    [Crossref] [Google Scholar]
  33. 33.
    Hogg JR. 2016.. Viral evasion and manipulation of host RNA quality control pathways. . J. Virol. 90::701018
    [Crossref] [Google Scholar]
  34. 34.
    Howard BE, Hu Q, Babaoglu AC, Chandra M, Borghi M, et al. 2013.. High-throughput RNA sequencing of Pseudomonas-infected Arabidopsis reveals hidden transcriptome complexity and novel splice variants. . PLOS ONE 8::e74183
    [Crossref] [Google Scholar]
  35. 35.
    Huang J, Gu L, Zhang Y, Yan T, Kong G, et al. 2017.. An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. . Nat. Commun. 8::2051
    [Crossref] [Google Scholar]
  36. 36.
    Huang J, Lu X, Wu H, Xie Y, Peng Q, et al. 2020.. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity. . Mol. Plant 13::147084
    [Crossref] [Google Scholar]
  37. 37.
    Jabre I, Chaudhary S, Guo W, Kalyna M, Reddy ASN, et al. 2021.. Differential nucleosome occupancy modulates alternative splicing in Arabidopsis thaliana. . New Phytol. 229::193745
    [Crossref] [Google Scholar]
  38. 38.
    Jeong B, Lin Y, Joe A, Guo M, Korneli C, et al. 2011.. Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. . J. Biol. Chem. 286::4327281
    [Crossref] [Google Scholar]
  39. 39.
    Jia J, Long Y, Zhang H, Li Z, Liu Z, et al. 2020.. Post-transcriptional splicing of nascent RNA contributes to widespread intron retention in plants. . Nat. Plants 6::78088
    [Crossref] [Google Scholar]
  40. 40.
    Jin Y, Gu T, Li X, Liu H, Han G, et al. 2022.. Characterization of a new splicing variant of powdery mildew resistance gene Pm4 in synthetic hexaploid wheat YAV249. . Front. Plant Sci. 13::1048252
    [Crossref] [Google Scholar]
  41. 41.
    Jung HW, Panigrahi GK, Jung GY, Lee YJ, Shin KH, et al. 2020.. Pathogen-associated molecular pattern-triggered immunity involves proteolytic degradation of core nonsense-mediated mRNA decay factors during the early defense response. . Plant Cell 32::1081101
    [Crossref] [Google Scholar]
  42. 42.
    Kalyna M, Simpson CG, Syed NH, Lewandowska D, Marquez Y, et al. 2012.. Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. . Nucleic Acids Res. 40::245469
    [Crossref] [Google Scholar]
  43. 43.
    Koncz C, Dejong F, Villacorta N, Szakonyi D, Koncz Z. 2012.. The spliceosome-activating complex: molecular mechanisms underlying the function of a pleiotropic regulator. . Front. Plant Sci. 3::9
    [Crossref] [Google Scholar]
  44. 44.
    Kornblihtt AR, de la Mata M, Fededa JP, Munoz MJ, Nogues G. 2004.. Multiple links between transcription and splicing. . RNA 10::148998
    [Crossref] [Google Scholar]
  45. 45.
    Kornblihtt AR, Schor IE, Alló M, Dujardin G, Petrillo E, Muñoz MJ. 2013.. Alternative splicing: a pivotal step between eukaryotic transcription and translation. . Nat. Rev. Mol. Cell Biol. 14::15365
    [Crossref] [Google Scholar]
  46. 46.
    Kufel J, Diachenko N, Golisz A. 2022.. Alternative splicing as a key player in the fine-tuning of the immunity response in Arabidopsis. . Mol. Plant Pathol. 23::122638
    [Crossref] [Google Scholar]
  47. 47.
    Kurihara Y, Matsui A, Hanada K, Kawashima M, Ishida J, et al. 2009.. Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. . PNAS 106::245358
    [Crossref] [Google Scholar]
  48. 48.
    Laloum T, Martín G, Duque P. 2018.. Alternative splicing control of abiotic stress responses. . Trends Plant Sci. 23::14050
    [Crossref] [Google Scholar]
  49. 49.
    Laskar P, Hazra A, Pal A, Kundu A. 2023.. Deciphering the role of alternative splicing as modulators of defense response in the MYMIV-Vigna mungo pathosystem. . Physiol. Plant 175::e13922
    [Crossref] [Google Scholar]
  50. 50.
    Li F, Wang A. 2018.. RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors. . PLOS Pathog. 14::e1007228
    [Crossref] [Google Scholar]
  51. 51.
    Li F, Wang A. 2019.. RNA-targeted antiviral immunity: more than just RNA silencing. . Trends Microbiol. 27::792805
    [Crossref] [Google Scholar]
  52. 52.
    Liang D, Yu J, Song T, Zhang R, Du Y, et al. 2022.. A genome-wide alternative splicing landscape specifically associated with durable rice blast resistance. . Agronomy 12::2414
    [Crossref] [Google Scholar]
  53. 53.
    Liu J, Chen X, Liang X, Zhou X, Yang F, et al. 2016.. Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense. . Plant Physiol. 171::142742
    [Google Scholar]
  54. 54.
    Lopato S, Forstner C, Kalyna M, Hilscher J, Langhammer U, et al. 2002.. Network of interactions of a novel plant-specific Arg/Ser-rich protein, atRSZ33, with atSC35-like splicing factors. . J. Biol. Chem. 277::3998998
    [Crossref] [Google Scholar]
  55. 55.
    Lu X, Yang Z, Song W, Si J, Yin Z, et al. 2021.. A novel Phytophthora sojae effector PsFYVE1 modulates transcription and alternative splicing of immunity related genes by targeting host RZ-1A protein. . bioRxiv 470886. https://doi.org/10.1101/2021.12.02.470886
  56. 56.
    Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. 2011.. Epigenetics in alternative pre-mRNA splicing. . Cell 144::1626
    [Crossref] [Google Scholar]
  57. 57.
    Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. 2010.. Regulation of alternative splicing by histone modifications. . Science 327::9961000
    [Crossref] [Google Scholar]
  58. 58.
    Ma J-Q, Xu W, Xu F, Lin A, Sun W, et al. 2020.. Differential alternative splicing genes and isoform regulation networks of rapeseed (Brassica napus L.) infected with Sclerotinia sclerotiorum. . Genes 11::784
    [Crossref] [Google Scholar]
  59. 59.
    Maor GL, Yearim A, Ast G. 2015.. The alternative role of DNA methylation in splicing regulation. . Trends Genet. 31::27480
    [Crossref] [Google Scholar]
  60. 60.
    Marquez Y, Brown JWS, Simpson C, Barta A, Kalyna M. 2012.. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. . Genome Res. 22::118495
    [Crossref] [Google Scholar]
  61. 61.
    Mejias J, Bazin J, Truong N-M, Chen Y, Marteu N, et al. 2020.. The root-knot nematode effector MiEFF18 interacts with the plant core spliceosomal protein SmD1 required for giant cell formation. . New Phytol. 229::340823
    [Crossref] [Google Scholar]
  62. 62.
    Meng Y, Shao C, Ma X, Wang H. 2013.. Introns targeted by plant microRNAs: a possible novel mechanism of gene regulation. . Rice 6::8
    [Crossref] [Google Scholar]
  63. 63.
    Mérai Z, Benkovics AH, Nyikó T, Debreczeny M, Hiripi L, et al. 2013.. The late steps of plant nonsense-mediated mRNA decay. . Plant J. 73::5062
    [Crossref] [Google Scholar]
  64. 64.
    Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, et al. 2010.. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. . Plant Physiol. 153::116174
    [Crossref] [Google Scholar]
  65. 65.
    Nicaise V, Joe A, Jeong B, Korneli C, Boutrot F, et al. 2013.. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. . EMBO J. 32::70112
    [Crossref] [Google Scholar]
  66. 66.
    Niyikiza D, Piya S, Routray P, Miao L, Kim WS, et al. 2020.. Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity. . Plant J. 103::174466
    [Crossref] [Google Scholar]
  67. 67.
    Palusa SG, Ali GS, Reddy ASN. 2007.. Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. . Plant J. 49::1091107
    [Crossref] [Google Scholar]
  68. 68.
    Peng Y, Bartley LE, Chen X, Dardick C, Chern M, et al. 2008.. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. . Mol. Plant 1::44658
    [Crossref] [Google Scholar]
  69. 69.
    Piya S, Hawk T, Patel B, Baldwin L, Rice JH, et al. 2022.. Kinase-dead mutation: a novel strategy for improving soybean resistance to soybean cyst nematode Heterodera glycines. . Mol. Plant Pathol. 23::41730
    [Crossref] [Google Scholar]
  70. 70.
    Piya S, Lopes-Caitar VS, Kim WS, Pantalone V, Krishnan HB, Hewezi T. 2021.. Hypermethylation of miRNA genes during nodule development. . Front. Mol. Biosci. 8::616623
    [Crossref] [Google Scholar]
  71. 71.
    Plaschka C, Lin P-C, Charenton C, Nagai K. 2018.. Prespliceosome structure provides insights into spliceosome assembly and regulation. . Nature 559::41922
    [Crossref] [Google Scholar]
  72. 72.
    Pradeepa MM, Sutherland HG, Ule J, Grimes GR, Bickmore WA. 2012.. Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. . PLOS Genet. 8::e1002717
    [Crossref] [Google Scholar]
  73. 73.
    Qiao Y, Shi J, Zhai Y, Hou Y, Ma W. 2015.. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. . PNAS 112::585055
    [Crossref] [Google Scholar]
  74. 74.
    Qin N, Zhang R, Zhang M, Niu Y, Fu S, et al. 2020.. Global profiling of dynamic alternative splicing modulation in Arabidopsis root upon Ralstonia solanacearum infection. . Genes 11::1078
    [Crossref] [Google Scholar]
  75. 75.
    Rambani A, Pantalone V, Yang S, Rice JH, Song Q, et al. 2020.. Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. . New Phytol. 227::16884
    [Crossref] [Google Scholar]
  76. 76.
    Raxwal VK, Simpson CG, Gloggnitzer J, Entinze JC, Guo W, et al. 2020.. Nonsense-mediated RNA decay factor UPF1 is critical for posttranscriptional and translational gene regulation in Arabidopsis. . Plant Cell 32::272541
    [Crossref] [Google Scholar]
  77. 77.
    Rayson S, Arciga-Reyes L, Wootton L, De Torres Zabala M, Truman W, et al. 2012.. A role for nonsense-mediated mRNA decay in plants: Pathogen responses are induced in Arabidopsis thaliana NMD mutants. . PLOS ONE 7::e31917
    [Crossref] [Google Scholar]
  78. 78.
    Reddy ASN, Marquez Y, Kalyna M, Barta A. 2013.. Complexity of the alternative splicing landscape in plants. . Plant Cell 25::365783
    [Crossref] [Google Scholar]
  79. 79.
    Riehs-Kearnan N, Gloggnitzer J, Dekrout B, Jonak C, Riha K. 2012.. Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. . Nucleic Acids Res. 40::561524
    [Crossref] [Google Scholar]
  80. 80.
    Rigo R, Bazin J, Crespi M, Charon C. 2019.. Alternative splicing in the regulation of plant–microbe interactions. . Plant Cell Physiol. 60::190616
    [Crossref] [Google Scholar]
  81. 81.
    Rogozin IB, Carmel L, Csuros M, Koonin EV. 2012.. Origin and evolution of spliceosomal introns. . Biol. Direct 7::11
    [Crossref] [Google Scholar]
  82. 82.
    Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M, et al. 2015.. Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and Rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. . Mol. Cell. Proteom. 14::55671
    [Crossref] [Google Scholar]
  83. 83.
    Sanabria NM, Dubery IA. 2016.. Alternative splicing of the receptor-like kinase Nt-Sd-RLK in tobacco cells responding to lipopolysaccharides: suggestive of a role in pathogen surveillance and perception?. FEBS Lett. 590::362838
    [Crossref] [Google Scholar]
  84. 84.
    Sánchez-Martín J, Widrig V, Herren G, Wicker T, Zbinden H, et al. 2021.. Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. . Nat. Plants 7::32741
    [Crossref] [Google Scholar]
  85. 85.
    Schor IE, Llères D, Risso GJ, Pawellek A, Ule J, et al. 2012.. Perturbation of chromatin structure globally affects localization and recruitment of splicing factors. . PLOS ONE 7::e48084
    [Crossref] [Google Scholar]
  86. 86.
    Schornack S, Ballvora A, Gürlebeck D, Peart J, Ganal M, et al. 2004.. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. . Plant J. 37::4660
    [Crossref] [Google Scholar]
  87. 87.
    Shang X, Cao Y, Ma L. 2017.. Alternative splicing in plant genes: a means of regulating the environmental fitness of plants. . Int. J. Mol. Sci. 18::432
    [Crossref] [Google Scholar]
  88. 88.
    Shen Q-H, Saijo Y, Mauch S, Biskup C, Bieri S, et al. 2007.. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. . Science 315::1098103
    [Crossref] [Google Scholar]
  89. 89.
    Shen Y, Zhou Z, Wang Z, Li W, Fang C, et al. 2014.. Global dissection of alternative splicing in paleopolyploid soybean. . Plant Cell 26::9961008
    [Crossref] [Google Scholar]
  90. 90.
    Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, et al. 2003.. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. . PNAS 100::912833
    [Crossref] [Google Scholar]
  91. 91.
    Stankovic N, Schloesser M, Joris M, Sauvage E, Hanikenne M, Motte P. 2016.. Dynamic distribution and interaction of the Arabidopsis SRSF1 subfamily splicing factors. . Plant Physiol. 170::100013
    [Crossref] [Google Scholar]
  92. 92.
    Streitner C, Köster T, Simpson CG, Shaw P, Danisman S, et al. 2012.. An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana. . Nucleic Acids Res. 40::1124055
    [Crossref] [Google Scholar]
  93. 93.
    Sun B, Huang J, Gao C, Li K, Zhao F, et al. 2023.. Alternative splicing of a potato disease resistance gene maintains homeostasis between development and immunity, and functions as a novel process for pathogen surveillance. . bioRxiv 544375. https://doi.org/10.1101/2023.06.09.544375
  94. 94.
    Tanabe N, Yoshimura K, Kimura A, Yabuta Y, Shigeoka S. 2007.. Differential expression of alternatively spliced mRNAs of Arabidopsis SR protein homologs, atSR30 and atSR45a, in response to environmental stress. . Plant Cell Physiol. 48::103649
    [Crossref] [Google Scholar]
  95. 95.
    Tang C, Xu Q, Zhao J, Yue M, Wang J, et al. 2022.. A rust fungus effector directly binds plant pre-mRNA splice site to reprogram alternative splicing and suppress host immunity. . Plant Biotechnol. J. 20::116781
    [Crossref] [Google Scholar]
  96. 96.
    Tang F, Yang S, Gao M, Zhu H. 2013.. Alternative splicing is required for RCT1-mediated disease resistance in Medicago truncatula. . Plant Mol. Biol. 82::36774
    [Crossref] [Google Scholar]
  97. 97.
    Thatcher SR, Zhou W, Leonard A, Wang B-B, Beatty M, et al. 2014.. Genome-wide analysis of alternative splicing in Zea mays: landscape and genetic regulation. . Plant Cell 26::347287
    [Crossref] [Google Scholar]
  98. 98.
    Tillemans V, Dispa L, Remacle C, Collinge M, Motte P. 2005.. Functional distribution and dynamics of Arabidopsis SR splicing factors in living plant cells. . Plant J. 41::56782
    [Crossref] [Google Scholar]
  99. 99.
    Tillemans V, Leponce I, Rausin G, Dispa L, Motte P. 2006.. Insights into nuclear organization in plants as revealed by the dynamic distribution of Arabidopsis SR splicing factors. . Plant Cell 18::321834
    [Crossref] [Google Scholar]
  100. 100.
    van Bentem SDLF, Anrather D, Roitinger E, Djamei A, Hufnagl T, et al. 2006.. Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. . Nucleic Acids Res. 34::326778
    [Crossref] [Google Scholar]
  101. 101.
    van den Hoogenhof MMG, Pinto YM, Creemers EE. 2016.. RNA splicing: regulation and dysregulation in the heart. . Circ. Res. 118::45468
    [Crossref] [Google Scholar]
  102. 102.
    van der Vossen E, Sikkema A, Hekkert BL, Gros J, Stevens P, et al. 2003.. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. . Plant J. 36::86782
    [Crossref] [Google Scholar]
  103. 103.
    Verma A, Lee C, Morriss S, Odu F, Kenning C, et al. 2018.. The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites. . New Phytol. 219::697713
    [Crossref] [Google Scholar]
  104. 104.
    Wang B-B, Brendel V. 2004.. The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. . Genome Biol. 5::R102
    [Crossref] [Google Scholar]
  105. 105.
    Wang X, Hu L, Wang X, Li N, Xu C, et al. 2016.. DNA methylation affects gene alternative splicing in plants: an example from rice. . Mol. Plant 9::3057
    [Crossref] [Google Scholar]
  106. 106.
    Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B. 1994.. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. . Cell 78::110115
    [Crossref] [Google Scholar]
  107. 107.
    Will CL, Lührmann R. 2011.. Spliceosome structure and function. . Cold Spring Harb. Perspect. Biol. 3::a003707
    [Crossref] [Google Scholar]
  108. 108.
    Wirthmueller L, Zhang Y, Jones JDG, Parker JE. 2007.. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. . Curr. Biol. 17::202329
    [Crossref] [Google Scholar]
  109. 109.
    Wu K, Fu Y, Ren Y, Liu L, Zhang X, Ruan M. 2023.. Turnip crinkle virus-encoded suppressor of RNA silencing suppresses mRNA decay by interacting with Arabidopsis XRN4. . Plant J. 116::74455
    [Crossref] [Google Scholar]
  110. 110.
    Yang S, Tang F, Zhu H. 2014.. Alternative splicing in plant immunity. . Int. J. Mol. Sci. 15::1042445
    [Crossref] [Google Scholar]
  111. 111.
    Yang XZ, Zhang HY, Li L. 2012.. Alternative mRNA processing increases the complexity of microRNA-based gene regulation in Arabidopsis. . Plant J. 70::42131
    [Crossref] [Google Scholar]
  112. 112.
    Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, et al. 2013.. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. . J. Exp. Bot. 64::508597
    [Crossref] [Google Scholar]
  113. 113.
    Zeng Z, Liu Y, Feng X-Y, Li S-X, Jiang X-M, et al. 2023.. The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network. . Plant Commun. 4::100429
    [Crossref] [Google Scholar]
  114. 114.
    Zhang F, Ke J, Zhang L, Chen R, Sugimoto K, et al. 2017.. Structural insights into alternative splicing-mediated desensitization of jasmonate signaling. . PNAS 114::172025
    [Crossref] [Google Scholar]
  115. 115.
    Zhang G, Guo G, Hu X, Zhang Y, Li Q, et al. 2010.. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. . Genome Res. 20::64654
    [Crossref] [Google Scholar]
  116. 116.
    Zhang H, Mao R, Wang Y, Zhang L, Wang C, et al. 2019.. Transcriptome-wide alternative splicing modulation during plant-pathogen interactions in wheat. . Plant Sci. 288::110160
    [Crossref] [Google Scholar]
  117. 117.
    Zhang X-C, Gassmann W. 2003.. RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. . Plant Cell 15::233342
    [Crossref] [Google Scholar]
  118. 118.
    Zhang X-C, Gassmann W. 2007.. Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. . Plant Physiol. 145::157787
    [Crossref] [Google Scholar]
  119. 119.
    Zhang X-N, Mo C, Garrett WM, Cooper B. 2014.. Phosphothreonine 218 is required for the function of SR45.1 in regulating flower petal development in Arabidopsis. . Plant Signal. Behav. 9::e29134
    [Crossref] [Google Scholar]
  120. 120.
    Zhang X-N, Mount SM. 2009.. Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development. . Plant Physiol. 150::145058
    [Crossref] [Google Scholar]
  121. 121.
    Zheng Y, Wang Y, Ding B, Fei Z. 2017.. Comprehensive transcriptome analyses reveal that potato spindle tuber viroid triggers genome-wide changes in alternative splicing, inducible trans-acting activity of phased secondary small interfering RNAs, and immune responses. . J. Virol. 91::e00247-17
    [Google Scholar]
  122. 122.
    Zhou T, He Y, Zeng X, Cai B, Qu S, Wang S. 2022.. Comparative analysis of alternative splicing in two contrasting apple cultivars defense against Alternaria alternata apple pathotype infection. . Int. J. Mol. Sci. 23::14202
    [Crossref] [Google Scholar]
  123. 123.
    Zhou Y, Lu Q, Zhang J, Zhang S, Weng J, et al. 2022.. Genome-wide profiling of alternative splicing and gene fusion during Rice black-streaked dwarf virus stress in maize (Zea mays L.). . Genes 13::456
    [Crossref] [Google Scholar]
  124. 124.
    Zorin EA, Afonin AM, Kulaeva OA, Gribchenko ES, Shtark OY, Zhukov VA. 2020.. Transcriptome analysis of alternative splicing events induced by arbuscular mycorrhizal fungi (Rhizophagus irregularis) in pea (Pisum sativum L.) roots. . Plants 9::1700
    [Crossref] [Google Scholar]
  125. 125.
    Zuo N, Bai W-Z, Wei W-Q, Yuan T-L, Zhang D, et al. 2022.. Fungal CFEM effectors negatively regulate a maize wall-associated kinase by interacting with its alternatively spliced variant to dampen resistance. . Cell Rep. 41::111877
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-phyto-121423-041908
Loading
/content/journals/10.1146/annurev-phyto-121423-041908
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error