Cited by 160Plant-Microbe Interactions and ImmunityImmune Response and InflammationInsect-Plant Interactions and Control

The function of plant PR1 and other members of the CAP protein superfamily in plant–pathogen interactions

Open access
Han, Zhu, Xiong, Dianguang, Schneiter, Roger, Tian, Chengming·2023·Molecular Plant Pathology

Abstract

The pathogenesis‐related (PR) proteins of plants have originally been identified as proteins that are strongly induced upon biotic and abiotic stress. These proteins fall into 17 distinct classes (PR1–PR17). The mode of action of most of these PR proteins has been well characterized, except for PR1, which belongs to a widespread superfamily of proteins that share a common CAP domain. Proteins of this family are not only expressed in plants but also in humans and in many different pathogens, including phytopathogenic nematodes and fungi. These proteins are associated with a diverse range of physiological functions. However, their precise mode of action has remained elusive. The importance of these proteins in immune defence is illustrated by the fact that PR1 overexpression in plants results in increased resistance against pathogens. However, PR1‐like CAP proteins are also produced by pathogens and deletion of these genes results in reduced virulence, suggesting that CAP proteins can exert both defensive and offensive functions. Recent progress has revealed that plant PR1 is proteolytically cleaved to release a C‐terminal CAPE1 peptide, which is sufficient to activate an immune response. The release of this signalling peptide is blocked by pathogenic effectors to evade immune defence. Moreover, plant PR1 forms complexes with other PR family members, including PR5, also known as thaumatin, and PR14, a lipid transfer protein, to enhance the host's immune response. Here, we discuss possible functions of PR1 proteins and their interactors, particularly in light of the fact that these proteins can bind lipids, which have important immune signalling functions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/mpp.13320

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 154

  1. Abraham, A. & Chandler, D.E. (2017) Tracing the evolutionary history of the CAP superfamily of proteins using amino acid sequence homology and conservation of splice sites. Journal of Molecular Evolution, 85, 137– 157. 29071358
  2. Alexander, D., Goodman, R.M., Gut‐Rella, M., Glascock, C., Weymann, K., Friedrich, L. et al. (1993) Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis‐related protein 1a. Proceedings of the National Academy of Sciences of the United States of America, 90, 7327– 7331. 8346252 PMC47130
  3. Ashkenazy, H., Abadi, S., Martz, E., Chay, O., Mayrose, I., Pupko, T. et al. (2016) ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Research, 44, W344– W350. 27166375 PMC4987940
  4. Asojo, O.A. (2011) Structure of a two‐CAP‐domain protein from the human hookworm parasite Necator americanus. Acta Crystallographica. Section D, Biological Crystallography, 67, 455– 462. 21543848 PMC3087624
  5. Asojo, O.A., Koski, R.A. & Bonafe, N. (2011) Structural studies of human glioma pathogenesis‐related protein 1. Acta Crystallographica. Section D, Biological Crystallography, 67, 847– 855. 21931216 PMC3176621
  6. Backer, R., Naidoo, S. & van den Berg, N. (2019) The NONEXPRESSOR OF PATHOGENESIS‐RELATED GENES 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Frontiers in Plant Science, 10, 102. 30815005 PMC6381062
  7. Barnes, J., Anderson, L.A. & Phillipson, J.D. (2007) Herbal medicines. 3rd edition. London: Pharmaceutical Press.
  8. Baroni, R.M., Luo, Z., Darwiche, R., Hudspeth, E.M., Schneiter, R., Pereira, G.A.G. et al. (2017) Crystal structure of MpPR‐1i, a SCP/TAPS protein from Moniliophthora perniciosa, the fungus that causes witches' broom disease of cacao. Scientific Reports, 7, 7818. 28798297 PMC5552782
  9. Bigeard, J., Colcombet, J. & Hirt, H. (2015) Signaling mechanisms in pattern‐triggered immunity (PTI). Molecular Plant, 8, 521– 539. 25744358
  10. Blein, J.P., Coutos‐Thévenot, P., Marion, D. & Ponchet, M. (2002) From elicitins to lipid‐transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends in Plant Science, 7, 293– 296. 12119165
  11. Breen, S., Williams, S.J., Winterberg, B., Kobe, B. & Solomon, P.S. (2016) Wheat PR‐1 proteins are targeted by necrotrophic pathogen effector proteins. The Plant Journal, 88, 13– 25. 27258471
  12. Breen, S., Williams, S.J., Outram, M., Kobe, B. & Solomon, P.S. (2017) Emerging insights into the functions of pathogenesis‐related protein 1. Trends in Plant Science, 22, 871– 879. 28743380
  13. Bücherl, C.A., Jarsch, I.K., Schudoma, C., Segonzac, C., Mbengue, M., Robatzek, S. et al. (2017) Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife, 6, e25114. 28262094 PMC5383397
  14. Cantacessi, C. & Gasser, R.B. (2012) SCP/TAPS proteins in helminths—Where to from now? Molecular and Cellular Probes, 26, 54– 59. 22005034
  15. Carafoli, E. & Krebs, J. (2016) Why calcium? How calcium became the best communicator. The Journal of Biological Chemistry, 291, 20849– 20857. 27462077 PMC5076498
  16. Carr, J.P., Dixon, D.C., Nikolau, B.J., Voelkerding, K.V. & Klessig, D.F. (1987) Synthesis and localization of pathogenesis‐related proteins in tobacco. Molecular and Cellular Biology, 7, 1580– 1583. 3299048 PMC365252
  17. Chaparro‐Garcia, A., Wilkinson, R.C., Gimenez‐Ibanez, S., Findlay, K., Coffey, M.D., Zipfel, C. et al. (2011) The receptor‐like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One, 6, e16608. 21304602 PMC3029390
  18. Chen, Y.L., Lee, C.Y., Cheng, K.T., Chang, W.H., Huang, R.N., Nam, H.G. et al. (2014) Quantitative peptidomics study reveals that a wound‐induced peptide from PR‐1 regulates immune signaling in tomato. The Plant Cell, 26, 4135– 4148. 25361956 PMC4247587
  19. Chien, P.S., Nam, H.G. & Chen, Y.R. (2015) A salt‐regulated peptide derived from the CAP superfamily protein negatively regulates salt‐stress tolerance in Arabidopsis. Journal of Experimental Botany, 66, 5301– 5313. 26093145 PMC4526916
  20. Choudhary, V. & Schneiter, R. (2012) Pathogen‐related yeast (PRY) proteins and members of the CAP superfamily are secreted sterol‐binding proteins. Proceedings of the National Academy of Sciences of the United States of America, 109, 16882– 16887. 23027975 PMC3479496
  21. Choudhary, V., Darwiche, R., Gfeller, D., Zoete, V., Michielin, O. & Schneiter, R. (2014) The caveolin‐binding motif of the pathogen‐related yeast protein Pry1, a member of the CAP protein superfamily, is required for in vivo export of cholesteryl acetate. Journal of Lipid Research, 55, 883– 894. 24598142 PMC3995466
  22. Christensen, S.A. & Kolomiets, M.V. (2011) The lipid language of plant–fungal interactions. Fungal Genetics and Biology, 48, 4– 14. 20519150
  23. Cottier, S., Darwiche, R., Meyenhofer, F., Debelyy, M.O. & Schneiter, R. (2020) The yeast cell wall protein Pry3 inhibits mating through highly conserved residues within the CAP domain. Biology Open, 9, bio053470. 32554483 PMC7340583
  24. Couet, J., Li, S., Okamoto, T., Ikezu, T. & Lisanti, M.P. (1997) Identification of peptide and protein ligands for the caveolin‐scaffolding domain. Implications for the interaction of caveolin with caveolae‐associated proteins. The Journal of Biological Chemistry, 272, 6525– 6533. 9045678
  25. Dahlin, P., Srivastava, V., Ekengren, S., McKee, L.S. & Bulone, V. (2017) Comparative analysis of sterol acquisition in the oomycetes Saprolegnia parasitica and Phytophthora infestans. PLoS One, 12, e0170873. 28152045 PMC5289490
  26. Darwiche, R. & Schneiter, R. (2016) Cholesterol‐binding by the yeast CAP family member, Pry1, requires the presence of an aliphatic side chain on cholesterol. Journal of Steroids and Hormonal Science, 7, 2.
  27. Darwiche, R., Kelleher, A., Hudspeth, E.M., Schneiter, R. & Asojo, O.A. (2016) Structural and functional characterization of the CAP domain of pathogen‐related yeast 1 (Pry1) protein. Scientific Reports, 6, 28838. 27344972 PMC4921858
  28. Darwiche, R., El Atab, O., Baroni, R.M., Teixeira, P.J.P.L., Mondego, J.M.C., Pereira, G.A.G. et al. (2017) Plant pathogenesis‐related proteins of the cacao fungal pathogen Moniliophthora perniciosa differ in their lipid‐binding specificities. The Journal of Biological Chemistry, 292, 20558– 20569. 29042440 PMC5733592
  29. Darwiche, R., Mène‐Saffrané, L., Gfeller, D., Asojo, O.A. & Schneiter, R. (2017) The pathogen‐related yeast protein Pry1, a member of the CAP protein superfamily, is a fatty acid‐binding protein. The Journal of Biological Chemistry, 292, 8304– 8314. 28365570 PMC5437237
  30. Darwiche, R., Lugo, F., Drurey, C., Varossieau, K., Smant, G., Wilbers, R.H.P. et al. (2018) Crystal structure of Brugia malayi venom allergen‐like protein‐1 (BmVAL‐1), a vaccine candidate for lymphatic filariasis. International Journal for Parasitology, 48, 371– 378. 29501266 PMC5893361
  31. Daum, G., Lees, N.D., Bard, M. & Dickson, R. (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast, 14, 1471– 1510. 9885152
  32. Derevnina, L., Dagdas, Y.F., de la Concepcion, J.C., Bialas, A., Kellner, R., Petre, B. et al. (2016) Nine things to know about elicitins. The New Phytologist, 212, 888– 895. 27582271
  33. Desmedt, W., Mangelinckx, S., Kyndt, T. & Vanholme, B. (2020) A phytochemical perspective on plant defense against nematodes. Frontiers in Plant Science, 11, 602079. 33281858 PMC7691236
  34. Dixon, D.C., Cutt, J.R. & Klessig, D.F. (1991) Differential targeting of the tobacco PR‐1 pathogenesis‐related proteins to the extracellular space and vacuoles of crystal idioblasts. The EMBO Journal, 10, 1317– 1324. 2026137 PMC452789
  35. Dokládal, L., Obořil, M., Stejskal, K., Zdráhal, Z., Ptáčková, N., Chaloupková, R. et al. (2012) Physiological and proteomic approaches to evaluate the role of sterol binding in elicitin‐induced resistance. Journal of Experimental Botany, 63, 2203– 2215. 22223811 PMC3295402
  36. Du, J., Verzaux, E., Chaparro‐Garcia, A., Bijsterbosch, G., Keizer, L.C., Zhou, J.I. et al. (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants, 1, 15034. 27247034
  37. Eberle, H.B., Serrano, R.L., Füllekrug, J., Schlosser, A., Lehmann, W.D., Lottspeich, F. et al. (2002) Identification and characterization of a novel human plant pathogenesis‐related protein that localizes to lipid‐enriched microdomains in the Golgi complex. Journal of Cell Science, 115, 827– 838. 11865038
  38. El Atab, O., Kocabey, A.E., Asojo, O.A. & Schneiter, R. (2022) Prostate secretory protein 94 inhibits sterol binding and export by the mammalian CAP protein CRISP2 in a calcium‐sensitive manner. The Journal of Biological Chemistry, 298, 101600. 35063506 PMC8857485
  39. Fang, Z., He, Y., Liu, Y., Jiang, W., Song, J. & Wang, S. (2020) Bioinformatic identification and analyses of the non‐specific lipid transfer proteins in wheat. Journal of Integrative Agriculture, 19, 1170– 1185.
  40. Fernandez, C., Szyperski, T., Bruyere, T., Ramage, P., Mosinger, E. & Wuthrich, K. (1997) NMR solution structure of the pathogenesis‐related protein P14a. Journal of Molecular Biology, 266, 576– 593. 9067611
  41. Frías, M., Brito, N. & González, C. (2013) The Botrytis cinerea cerato‐platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application. Molecular Plant Pathology, 14, 191– 196. 23072280 PMC6638659
  42. Fujiwara, M., Hamada, S., Hiratsuka, M., Fukao, Y., Kawasaki, T. & Shimamoto, K. (2009) Proteome analysis of detergent‐resistant membranes (DRMs) associated with OsRac1‐mediated innate immunity in rice. Plant & Cell Physiology, 50, 1191– 1200. 19502382 PMC2709549
  43. Gaikwad, A.S., Hu, J., Chapple, D.G. & O'Bryan, M.K. (2020) The functions of CAP superfamily proteins in mammalian fertility and disease. Human Reproduction Update, 26, 689– 723. 32378701
  44. Gamir, J., Darwiche, R., van't Hof, P., Choudhary, V., Stumpe, M., Schneiter, R. et al. (2017) The sterol‐binding activity of PATHOGENESIS‐RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein. The Plant Journal, 89, 502– 509. 27747953
  45. Gao, R., Ding, M., Jiang, S., Zhao, Z., Chenthamara, K., Shen, Q. et al. (2020) The evolutionary and functional paradox of cerato‐platanins in fungi. Applied and Environmental Microbiology, 86, e00696– e00620. 32332135 PMC7301859
  46. Ghorbel, M., Zribi, I., Missaoui, K., Drira‐Fakhfekh, M., Azzouzi, B. & Brini, F. (2021) Differential regulation of the durum wheat pathogenesis‐related protein (PR1) by calmodulin TdCaM1.3 protein. Molecular Biology Reports, 48, 347– 362. 33313970
  47. Gibbs, G.M., Roelants, K. & O'Bryan, M.K. (2008) The CAP superfamily: cysteine‐rich secretory proteins, antigen 5, and pathogenesis‐related 1 proteins—roles in reproduction, cancer, and immune defense. Endocrine Reviews, 29, 865– 897. 18824526
  48. Godfrey, D., Böhlenius, H., Pedersen, C., Zhang, Z., Emmersen, J. & Christensen, H. (2010). Powdery mildew fungal effector candidates share N‐terminal Y/F/WxC‐motif. BMC Genomics, 11, 317. 20487537 PMC2886064
  49. Granado, J., Felix, G. & Boller, T. (1995) Perception of fungal sterols in plants (subnanomolar concentrations of ergosterol elicit extracellular alkalinization in tomato cells). Plant Physiology, 107, 485– 490. 12228375 PMC157151
  50. Griebel, T. & Zeier, J. (2010) A role for β‐sitosterol to stigmasterol conversion in plant–pathogen interactions. The Plant Journal, 63, 254– 268. 20444228
  51. Gronnier, J., Gerbeau‐Pissot, P., Germain, V., Mongrand, S. & Simon‐Plas, F. (2018) Divide and rule: plant plasma membrane organization. Trends in Plant Science, 23, 899– 917. 30174194
  52. Guo, J., Bai, Y., Wei, Y., Dong, Y., Zeng, H., Reiter, R.J. et al. (2022) Fine‐tuning of pathogenesis‐related protein 1 (PR1) activity by the melatonin biosynthetic enzyme ASMT2 in defense response to cassava bacterial blight. Journal of Pineal Research, 72, e12784. 34936113
  53. Hakim, Ullah, A., Hussain, A., Shaban, M., Khan, A.H., Alariqi, M. et al. (2018) Osmotin: a plant defense tool against biotic and abiotic stresses. Plant Physiology and Biochemistry, 123, 149– 159. 29245030
  54. Han, X. & Kahmann, R. (2019) Manipulation of phytohormone pathways by effectors of filamentous plant pathogens. Frontiers in Plant Science, 10, 822. 31297126 PMC6606975
  55. Han, Z., Xiong, D., Xu, Z., Liu, T. & Tian, C. (2021) The Cytospora chrysosperma virulence effector CcCAP1 mainly localizes to the plant nucleus to suppress plant immune responses. mSphere, 6, e00883‐20– e00820. 33627507 PMC8544888
  56. Heath, M.C. (2000) Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology, 3, 315– 319. 10873843
  57. Ilyas, M., Hörger, A.C., Bozkurt, T.O., van den Burg, H.A., Kaschani, F., Kaiser, M. et al. (2015) Functional divergence of two secreted immune proteases of tomato. Current Biology, 25, 2300– 2306. 26299516
  58. Jones, J.D. & Dangl, J.L. (2006) The plant immune system. Nature, 444, 323– 329. 17108957
  59. Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H. et al. (1999) The small GTP‐binding protein rac is a regulator of cell death in plants. Proceedings of the National Academy of Sciences of the United States of America, 96, 10922– 10926. 10485927 PMC17984
  60. Kazan, K. & Gardiner, D.M. (2017) Targeting pathogen sterols: defence and counterdefence. PLoS Pathogens, 13, e1006297. 28542599 PMC5436867
  61. Khoza, T.G., Dubery, I.A. & Piater, L.A. (2019) Identification of candidate ergosterol‐responsive proteins associated with the plasma membrane of Arabidopsis thaliana. International Journal of Molecular Sciences, 20, E1302. PMC6471938 30875866
  62. Kirby, T.W., Mueller, G.A., DeRose, E.F., Lebetkin, M.S., Meiss, G., Pingoud, A. et al. (2002) The nuclease A inhibitor represents a new variation of the rare PR‐1 fold. Journal of Molecular Biology, 320, 771– 782. 12095254
  63. Klemptner, R.L., Sherwood, J.S., Tugizimana, F., Dubery, I.A. & Piater, L.A. (2014) Ergosterol, an orphan fungal microbe‐associated molecular pattern (MAMP). Molecular Plant Pathology, 15, 747– 761. 24528492 PMC6638689
  64. Kong, M., Sheng, T., Liang, J., Ali, Q., Gu, Q., Wu, H. et al. (2021) Melatonin and its homologs induce immune responses via receptors trP47363‐trP13076 in Nicotiana benthamiana. Frontiers in Plant Science, 12, 691835. 34276740 PMC8278317
  65. Kothari, K.S., Dansana, P.K., Giri, J. & Tyagi, A.K. (2016) Rice stress associated protein 1 (OsSAP1) interacts with aminotransferase (OsAMTR1) and pathogenesis‐related 1a protein (OsSCP) and regulates abiotic stress responses. Frontiers in Plant Science, 7, 1057. 27486471 PMC4949214
  66. Kourelis, J., Malik, S., Mattinson, O., Krauter, S., Kahlon, P.S., Paulus, J.K. et al. (2020) Evolution of a guarded decoy protease and its receptor in solanaceous plants. Nature Communications, 11, 4393. PMC7468133 32879321
  67. Lai, Z. & Mengiste, T. (2013) Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Current Opinion in Plant Biology, 16, 505– 512. 23859758
  68. Laird, J., Armengaud, P., Giuntini, P., Laval, V. & Milner, J.J. (2004) Inappropriate annotation of a key defence marker in Arabidopsis: will the real PR‐1 please stand up. Planta, 219, 1089– 1092. 15293050
  69. Levental, I., Levental, K.R. & Heberle, F.A. (2020) Lipid rafts: controversies resolved, mysteries remain. Trends in Cell Biology, 30, 341– 353. 32302547 PMC7798360
  70. Li, L., Yang, G., Ren, C., Tanimoto, R., Hirayama, T., Wang, J. et al. (2013) Glioma pathogenesis‐related protein 1 induces prostate cancer cell death through Hsc70‐mediated suppression of AURKA and TPX2. Molecular Oncology, 7, 484– 496. 23333597 PMC3907183
  71. Li, J., Xu, C., Yang, S., Chen, C., Tang, S., Wang, J. et al. (2021) A venom allergen‐like protein, RsVAP, the first discovered effector protein of Radopholus similis that inhibits plant defense and facilitates parasitism. International Journal of Molecular Sciences, 22, 4782. 33946385 PMC8125365
  72. Li, J., Ma, X., Wang, C., Liu, S., Yu, G., Gao, M. et al. (2022) Acetylation of a fungal effector that translocates host PR1 facilitates virulence. eLife, 11, e82628. 36374166 PMC9681213
  73. Li, Z.T., Dhekney, S.A. & Gray, D.J. (2011) PR‐1 gene family of grapevine: a uniquely duplicated PR‐1 gene from a Vitis interspecific hybrid confers high level resistance to bacterial disease in transgenic tobacco. Plant Cell Reports, 30, 1– 11. 20967449
  74. Lincoln, J.E., Sanchez, J.P., Zumstein, K. & Gilchrist, D.G. (2018) Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues. Molecular Plant Pathology, 19, 2111– 2123. 29603552 PMC6638019
  75. Lingwood, D. & Simons, K. (2010) Lipid rafts as a membrane‐organizing principle. Science, 327, 46– 50. 20044567
  76. Lochman, J. & Mikes, V. (2006) Ergosterol treatment leads to the expression of a specific set of defence‐related genes in tobacco. Plant Molecular Biology, 62, 43– 51. 16900324
  77. Lozano‐Torres, J.L., Wilbers, R.H.P., Gawronski, P., Boshoven, J.C., Finkers‐Tomczak, A., Cordewener, J.H.G. et al. (2012) Dual disease resistance mediated by the immune receptor Cf‐2 in tomato requires a common virulence target of a fungus and a nematode. Proceedings of the National Academy of Sciences of the United States of America, 109, 10119– 10124. 22675118 PMC3382537
  78. Lozano‐Torres, J.L., Wilbers, R.H.P., Warmerdam, S., Finkers‐Tomczak, A., Diaz‐Granados, A., van Schaik, C.C. et al. (2014) Apoplastic venom allergen‐like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLoS Pathogens, 10, e1004569. 25500833 PMC4263768
  79. Lu, S. & Edwards, M.C. (2018) Molecular characterization and functional analysis of PR‐1‐like proteins identified from the wheat head blight fungus Fusarium graminearum. Phytopathology, 108, 510– 520. 29117786
  80. Lu, S., Friesen, T.L. & Faris, J.D. (2011) Molecular characterization and genomic mapping of the pathogenesis‐related protein 1 (PR‐1) gene family in hexaploid wheat (Triticum aestivum L.). Molecular Genetics and Genomics, 285, 485– 503. 21516334
  81. Lu, S., Faris, J.D., Sherwood, R. & Edwards, M.C. (2013) Dimerization and protease resistance: new insight into the function of PR‐1. Journal of Plant Physiology, 170, 105– 110. 22921679
  82. Lu, S., Faris, J.D., Sherwood, R., Friesen, T.L. & Edwards, M.C. (2014) A dimeric PR‐1‐type pathogenesis‐related protein interacts with ToxA and potentially mediates ToxA‐induced necrosis in sensitive wheat. Molecular Plant Pathology, 15, 650– 663. 24433289 PMC6638811
  83. Lu, S., Faris, J.D. & Edwards, M.C. (2017) Molecular cloning and characterization of two novel genes from hexaploid wheat that encode double PR‐1 domains coupled with a receptor‐like protein kinase. Molecular Genetics and Genomics, 292, 435– 452. 28120099
  84. Luo, S., Liu, S., Kong, L., Peng, H., Huang, W., Jian, H. et al. (2019) Two venom allergen‐like proteins, HaVAP1 and HaVAP2, are involved in the parasitism of Heterodera avenae. Molecular Plant Pathology, 20, 471– 484. 30422356 PMC6637866
  85. Luo, X., Tian, T., Feng, L., Yang, X., Li, L., Tan, X. et al. (2023) Pathogenesis‐related protein 1 suppresses oomycete pathogen by targeting against AMPK kinase complex. Journal of Advanced Research, 43, 13– 26. 36585103 PMC9811325
  86. Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J. & Cameron, R.K. (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature, 419, 399– 403. 12353036
  87. Malinsky, J., Opekarova, M., Grossmann, G. & Tanner, W. (2013) Membrane microdomains, rafts, and detergent‐resistant membranes in plants and fungi. Annual Review of Plant Biology, 64, 501– 529. 23638827
  88. Mamode Cassim, A., Grison, M., Ito, Y., Simon‐Plas, F., Mongrand, S. & Boutté, Y. (2020) Sphingolipids in plants: a guidebook on their function in membrane architecture, cellular processes, and environmental or developmental responses. FEBS Letters, 594, 3719– 3738. 33151562
  89. McLaughlin, J.E., Al Darwish, N., Garcia‐Sanchez, J., Tyagi, N., Trick, H.N. & McCormick, S. (2020) A lipid transfer protein has antifungal and antioxidant activity and suppresses Fusarium head blight disease and DON accumulation in transgenic wheat. Phytopathology, 111, 671– 683. 32896217
  90. Meijer, H.J., Mancuso, F.M., Espadas, G., Seidl, M.F., Chiva, C., Govers, F. et al. (2014) Profiling the secretome and extracellular proteome of the potato late blight pathogen Phytophthora infestans. Molecular & Cellular Proteomics, 13, 2101– 2113. 24872595 PMC4125740
  91. Mendez, S., D'Samuel, A., Antoine, A.D., Ahn, S. & Hotez, P. (2008) Use of the air pouch model to investigate immune responses to a hookworm vaccine containing the Na‐ASP‐2 protein in rats. Parasite Immunology, 30, 53– 56. 18086017
  92. Mikes, V., Milat, M.L., Ponchet, M., Ricci, P. & Blein, J.P. (1997) The fungal elicitor cryptogein is a sterol carrier protein. FEBS Letters, 416, 190– 192. 9369212
  93. Milne, T.J., Abbenante, G., Tyndall, J.D., Halliday, J. & Lewis, R.J. (2003) Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis‐related protein superfamily. The Journal of Biological Chemistry, 278, 31105– 31110. 12759345
  94. Misas Villamil, J.C., Mueller, A.N., Demir, F., Meyer, U., Ökmen, B., Schulze Hüynck, J. et al. (2019) A fungal substrate mimicking molecule suppresses plant immunity via an inter‐kingdom conserved motif. Nature Communications, 10, 1576. PMC6450895 30952847
  95. Missaoui, K., Gonzalez‐Klein, Z., Pazos‐Castro, D., Hernandez‐Ramirez, G., Garrido‐Arandia, M., Brini, F. et al. (2022) Plant non‐specific lipid transfer proteins: an overview. Plant Physiology and Biochemistry, 171, 115– 127. 34992048
  96. Nagano, M., Ishikawa, T., Fujiwara, M., Fukao, Y., Kawano, Y., Kawai‐Yamada, M. et al. (2016) Plasma membrane microdomains are essential for Rac1‐RbohB/H‐mediated immunity in rice. The Plant Cell, 28, 1966– 1983. 27465023 PMC5006704
  97. Niderman, T., Genetet, I., Bruyere, T., Gees, R., Stintzi, A., Legrand, M. et al. (1995) Pathogenesis‐related PR‐1 proteins are antifungal. isolation and characterization of three 14‐kilodalton proteins of tomato and of a basic PR‐1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiology, 108, 17– 27. 7784503 PMC157301
  98. Nolan, T.M., Vukašinović, N., Liu, D., Russinova, E. & Yin, Y. (2020) Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. The Plant Cell, 32, 295– 318. 31776234 PMC7008487
  99. Noman, A., Aqeel, M., Irshad, M.K., Qari, S.H., Hashem, M., Alamri, S. et al. (2020) Elicitins as molecular weapons against pathogens: consolidated biotechnological strategy for enhancing plant growth. Critical Reviews in Biotechnology, 40, 821– 832. 32546015
  100. Oliver, R.P., Friesen, T.L., Faris, J.D. & Solomon, P.S. (2012) Stagonospora nodorum: from pathology to genomics and host resistance. Annual Review of Phytopathology, 50, 23– 43. 22559071
  101. Osman, H., Vauthrin, S., Mikes, V., Milat, M.L., Panabières, F., Marais, A. et al. (2001) Mediation of elicitin activity on tobacco is assumed by elicitin‐sterol complexes. Molecular Biology of the Cell, 12, 2825– 2834. 11553720 PMC59716
  102. Pandelova, I., Figueroa, M., Wilhelm, L.J., Manning, V.A., Mankaney, A.N., Mockler, T.C. et al. (2012) Host‐selective toxins of Pyrenophora tritici‐repentis induce common responses associated with host susceptibility. PLoS One, 7, e40240. 22792250 PMC3391247
  103. Paulus, J.K., Kourelis, J., Ramasubramanian, S., Homma, F., Godson, A., Hörger, A.C. et al. (2020) Extracellular proteolytic cascade in tomato activates immune protease Rcr3. Proceedings of the National Academy of Sciences of the United States of America, 117, 17409– 17417. 32616567 PMC7382257
  104. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. et al. (2004) UCSF chimera—a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605– 1612. 15264254
  105. Ponchet, M., Panabières, F., Milat, M.L., Mikes, V., Montillet, J.L., Suty, L. et al. (1999) Are elicitins cryptograms in plant–oomycete communications. Cellular and Molecular Life Sciences, 56, 1020– 1047. 11212320 PMC11147014
  106. Prados‐Rosales, R.C., Roldán‐Rodríguez, R., Serena, C., López‐Berges, M.S., Guarro, J., Martínez‐del‐Pozo, Á. et al. (2012) A PR‐1‐like protein of Fusarium oxysporum functions in virulence on mammalian hosts. The Journal of Biological Chemistry, 287, 21970– 21979. 22553200 PMC3381157
  107. Rauscher, M., Adam, A.L., Wirtz, S., Guggenheim, R., Mendgen, K. & Deising, H.B. (1999) PR‐1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. The Plant Journal, 19, 625– 633. 10571848
  108. Rooney, H.C., Van't Klooster, J.W., van der Hoorn, R.A., Joosten, M.H., Jones, J.D. & de Wit, P.J. (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf‐2‐dependent disease resistance. Science, 308, 1783– 1786. 15845874
  109. Rossard, S., Roblin, G. & Atanassova, R. (2010) Ergosterol triggers characteristic elicitation steps in Beta vulgaris leaf tissues. Journal of Experimental Botany, 61, 1807– 1816. 20304987
  110. Salminen, T.A., Blomqvist, K. & Edqvist, J. (2016) Lipid transfer proteins: classification, nomenclature, structure, and function. Planta, 244, 971– 997. 27562524 PMC5052319
  111. Sandor, R., Der, C., Grosjean, K., Anca, I., Noirot, E., Leborgne‐Castel, N. et al. (2016) Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence. Journal of Experimental Botany, 67, 5173– 5185. 27604805 PMC5014163
  112. Sarowar, S., Kim, Y.J., Kim, E.N., Kim, K.D., Hwang, B.K., Islam, R. et al. (2005) Overexpression of a pepper basic pathogenesis‐related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Reports, 24, 216– 224. 15719238
  113. Saur, I.M.L. & Hückelhoven, R. (2021) Recognition and defence of plant‐infecting fungal pathogens. Journal of Plant Physiology, 256, 153324. 33249386
  114. Schneiter, R. & Di Pietro, A. (2013) The CAP protein superfamily: function in sterol export and fungal virulence. Biomolecular Concepts, 4, 519– 525. 25436594
  115. Seo, P.J., Lee, A.‐K., Xiang, F. & Park, C.‐M. (2008) Molecular and functional profiling of Arabidopsis pathogenesis‐related genes: insights into their roles in salt response of seed germination. Plant and Cell Physiology, 49, 334– 344. 18203731
  116. Sessa, G., Yang, X.Q., Raz, V., Eyal, Y. & Fluhr, R. (1995) Dark induction and subcellular localization of the pathogenesis‐related PRB‐1b protein. Plant Molecular Biology, 28, 537– 547. 7632922
  117. Sharfman, M., Bar, M., Schuster, S., Leibman, M. & Avni, A. (2014) Sterol‐dependent induction of plant defense responses by a microbe‐associated molecular pattern from Trichoderma viride. Plant Physiology, 164, 819– 827. 24351686 PMC3912108
  118. Shin, S.H., Pak, J.H., Kim, M.J., Kim, H.J., Oh, J.S., Choi, H.K. et al. (2014) An acidic PATHOGENESIS‐RELATED1 gene of Oryza grandiglumis is involved in disease resistance response against bacterial infection. Plant Pathology Journal, 30, 208– 214. 25289005 PMC4174849
  119. Shoji‐Kawata, S., Sumpter, R., Leveno, M., Campbell, G.R., Zou, Z., Kinch, L. et al. (2013) Identification of a candidate therapeutic autophagy‐inducing peptide. Nature, 494, 201– 206. 23364696 PMC3788641
  120. Siebers, M., Brands, M., Wewer, V., Duan, Y., Hölzl, G. & Dörmann, P. (2016) Lipids in plant–microbe interactions. Biochimica et Biophysica Acta, 1861, 1379– 1395. 26928590
  121. Smant, G., Helder, J. & Goverse, A. (2018) Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes. The Plant Journal, 93, 686– 702. 29277939
  122. Song, Y., Liu, W., Zhao, Y., Zang, J. & Gao, H. (2021) Fumonisin B1 exposure induces apoptosis of human kidney tubular epithelial cells through regulating PTEN/PI3K/AKT signaling pathway via disrupting lipid raft formation. Toxicon, 204, 31– 36. 34740561
  123. Starý, T., Satková, P., Piterková, J., Mieslerová, B., Luhová, L., Mikulík, J. et al. (2019) The elicitin β‐cryptogein's activity in tomato is mediated by jasmonic acid and ethylene signalling pathways independently of elicitin‐sterol interactions. Planta, 249, 739– 749. 30374914
  124. Sun, J.Y., Gaudet, D.A., Lu, Z.X., Frick, M., Puchalski, B. & Laroche, A. (2008) Characterization and antifungal properties of wheat nonspecific lipid transfer proteins. Molecular Plant‐Microbe Interactions, 21, 346– 360. 18257684
  125. Sung, Y.C., Outram, M.A., Breen, S., Wang, C., Dagvadorj, B., Winterberg, B. et al. (2021) PR1‐mediated defence via C‐terminal peptide release is targeted by a fungal pathogen effector. The New Phytologist, 229, 3467– 3480. 33277705
  126. Szyperski, T., Fernandez, C., Mumenthaler, C. & Wuthrich, K. (1998) Structure comparison of human glioma pathogenesis‐related protein GliPR and the plant pathogenesis‐related protein P14a indicates a functional link between the human immune system and a plant defense system. Proceedings of the National Academy of Sciences of the United States of America, 95, 2262– 2266. 9482873 PMC19313
  127. Tadokoro, T., Modahl, C.M., Maenaka, K. & Aoki‐Shioi, N. (2020) Cysteine‐rich secretory proteins (CRISPs) from venomous snakes: an overview of the functional diversity in a large and underappreciated superfamily. Toxins, 12, E175. PMC7150914 32178374
  128. Tanaka, K. & Heil, M. (2021) Damage‐associated molecular patterns (DAMPs) in plant innate immunity: applying the danger model and evolutionary perspectives. Annual Review of Phytopathology, 59, 53– 75. 33900789
  129. Teixeira, P.J., Thomazella, D.P., Vidal, R.O., Do Prado, P.F., Reis, O., Baroni, R.M. et al. (2012) The fungal pathogen Moniliophthora perniciosa has genes similar to plant PR‐1 that are highly expressed during its interaction with cacao. PLoS One, 7, e45929. 23029323 PMC3447762
  130. Teixeira, P.J., Costa, G.G., Fiorin, G.L., Pereira, G.A. & Mondego, J.M. (2013) Novel receptor‐like kinases in cacao contain PR‐1 extracellular domains. Molecular Plant Pathology, 14, 602– 609. 23573899 PMC6638629
  131. Valitova, J., Sulkarnayeva, A., Kotlova, E., Ponomareva, A., Mukhitova, F.K., Murtazina, L. et al. (2014) Sterol binding by methyl‐β‐cyclodextrin and nystatin‐‐comparative analysis of biochemical and physiological consequences for plants. The FEBS Journal, 281, 2051– 2060. 24612537
  132. Van Galen, J., Van Balkom, B.W., Serrano, R.L., Kaloyanova, D., Eerland, R., Stüven, E. et al. (2010) Binding of GAPR‐1 to negatively charged phospholipid membranes: unusual binding characteristics to phosphatidylinositol. Molecular Membrane Biology, 27, 81– 91. 20095951
  133. van Loon, L.C. & van Kammen, A. (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. “Samsun” and “Samsun NN”. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 190– 211. 4191688
  134. van Loon, L.C., Rep, M. & Pieterse, C.M. (2006) Significance of inducible defense‐related proteins in infected plants. Annual Review of Phytopathology, 44, 135– 162. 16602946
  135. Vatsa, P., Chiltz, A., Luini, E., Vandelle, E., Pugin, A. & Roblin, G. (2011) Cytosolic calcium rises and related events in ergosterol‐treated Nicotiana cells. Plant Physiology and Biochemistry, 49, 764– 773. 21530285
  136. Virdi, A.S., Singh, S. & Singh, P. (2015) Abiotic stress responses in plants: roles of calmodulin‐regulated proteins. Frontiers in Plant Science, 6, 809. 26528296 PMC4604306
  137. Wang, F., Shen, S., Zhao, C., Cui, Z., Meng, L., Wu, W. et al. (2022) TaPR1 interacts with TaTLP1 via the αIV helix to be involved in wheat defense to Puccinia triticina through the CAPE1 motif. Frontiers in Plant Science, 13, 874654. 35720612 PMC9199852
  138. Wang, F., Yuan, S., Wu, W., Yang, Y., Cui, Z., Wang, H. et al. (2020) TaTLP1 interacts with TaPR1 to contribute to wheat defense responses to leaf rust fungus. PLoS Genetics, 16, e1008713. 32658889 PMC7357741
  139. Wang, K., Senthil‐Kumar, M., Ryu, C.M., Kang, L. & Mysore, K.S. (2012) Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiology, 158, 1789– 1802. 22298683 PMC3320186
  140. Wang, X., Yang, B., Li, K., Kang, Z., Cantu, D. & Dubcovsky, J. (2016) A conserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis‐related genes in response to pathogens. Molecular Plant‐Microbe Interactions, 29, 977– 989. 27898286
  141. Wang, Y.L., Kuo, J.H., Lee, S.C., Liu, J.S., Hsieh, Y.C., Shih, Y.T. et al. (2010) Cobra CRISP functions as an inflammatory modulator via a novel Zn2+‐ and heparan sulfate‐dependent transcriptional regulation of endothelial cell adhesion molecules. The Journal of Biological Chemistry, 285, 37872– 37883. 20889969 PMC2988390
  142. Wangorsch, A., Scheurer, S., Blanca, M., Blanca‐Lopez, N., Somoza, M.L. & Martín‐Pedraza, L. (2022) Allergenic properties and molecular characteristics of PR‐1 proteins. Frontiers in Allergy, 3, 824717. 35386656 PMC8974740
  143. Wilbers, R.H.P., Schneiter, R., Holterman, M.H.M., Drurey, C., Smant, G., Asojo, O.A. et al. (2018) Secreted venom allergen‐like proteins of helminths: conserved modulators of host responses in animals and plants. PLoS Pathogens, 14, e1007300. 30335852 PMC6193718
  144. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C. & London, E. (2001) Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Journal of Biological Chemistry, 276, 33540– 33546. 11432870
  145. Xu, X., Francischetti, I.M., Lai, R., Ribeiro, J.M. & Andersen, J.F. (2012) Structure of protein having inhibitory disintegrin and leukotriene scavenging functions contained in single domain. The Journal of Biological Chemistry, 287, 10967– 10976. 22311975 PMC3322842
  146. Yang, G., Tang, L., Gong, Y., Xie, J., Fu, Y., Jiang, D. et al. (2018) A cerato‐platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. The New Phytologist, 217, 739– 755. 29076546
  147. Yuan, M., Jiang, Z., Bi, G., Nomura, K., Liu, M., Wang, Y. et al. (2021) Pattern‐recognition receptors are required for NLR‐mediated plant immunity. Nature, 592, 105– 109. 33692546 PMC8016741
  148. Yuan, M., Ngou, B.P.M., Ding, P. & Xin, X.F. (2021) PTI‐ETI crosstalk: an integrative view of plant immunity. Current Opinion in Plant Biology, 62, 102030. 33684883
  149. Zhang, W.J., Pedersen, C., Kwaaitaal, M., Gregersen, P.L., Mørch, S.M., Hanisch, S. et al. (2012) Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Molecular Plant Pathology, 13, 1110– 1119. 22863200 PMC6638906
  150. Zhang, H., Mukherjee, M., Kim, J.E., Yu, W. & Shim, W.B. (2018) Fsr1, a striatin homologue, forms an endomembrane‐associated complex that regulates virulence in the maize pathogen Fusarium verticillioides. Molecular Plant Pathology, 19, 812– 826. 28467007 PMC6638083
  151. Zhang, J., Wang, F., Liang, F., Zhang, Y., Ma, L., Wang, H. et al. (2018) Functional analysis of a pathogenesis‐related thaumatin‐like protein gene TaLr35PR5 from wheat induced by leaf rust fungus. BMC Plant Biology, 18, 76. 29728059 PMC5935958
  152. Zhao, J., Bi, W., Zhao, S., Su, J., Li, M., Ma, L. et al. (2021) Wheat apoplast‐localized lipid transfer protein TaLTP3 enhances defense responses against Puccinia triticina. Frontiers in Plant Science, 12, 771806. 34899796 PMC8657149
  153. Zheng, Q., Putker, V. & Goverse, A. (2021) Molecular and cellular mechanisms involved in host‐specific resistance to cyst nematodes in crops. Frontiers in Plant Science, 12, 641582. 33767723 PMC7986850
  154. Zhu, X., Li, Z., Xu, H., Zhou, M., Du, L. & Zhang, Z. (2012) Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistances to Cochliobolus sativus and Fusarium graminearum in transgenic wheat. Functional & Integrative Genomics, 12, 481– 488. 22689341

Cited by

Sorted by citations

Authors
Han, Z., Xiong, D., Schneiter, R., & Tian, C.
Affiliations
  • University of Fribourg (CH)
  • Beijing Forestry University (CN)
Corresponding author
  • Xiong, Dianguang
  • Schneiter, Roger
Venue
Molecular Plant Pathology
Publisher
Wiley
Published
2023-03-17
Volume
24
Issue
6
Pages
651-668
ISSN
  • 1364-3703 (ISSN-L)
  • 1464-6722
OpenAlex
W4327811341
Cited by
160
References
2
Citations by year
2026: 53 · 2025: 52 · 2024: 44 · 2023: 10 · 2022: 1
FWCI
3.79
Type
journal article
Language
en
Open access
Locations
  • Molecular Plant Pathology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Greater South Information System
Funders
  • China Scholarship Council (202106510019)
  • National Natural Science Foundation of China (31800540)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030L_182725, 310030_207870, 31003A_173003)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords
pathogenesis-related proteins, PR1, plant-pathogen interaction, plant immunity, proteolytic cleavage, virulence, PR5, thaumatin, lipid transfer proteins, lipid binding, immune signaling, disease resistance
MeSH terms
Humans, Plant Diseases, Plant Proteins, Plants, Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review