Pathogenesis-related protein 10 in resistance to biotic stress: progress in elucidating functions, regulation and modes of action

Abstract

Introduction: The Family of pathogenesis-related proteins 10 (PR-10) is widely distributed in the plant kingdom. PR-10 are multifunctional proteins, constitutively expressed in all plant tissues, playing a role in growth and development or being induced in stress situations. Several studies have investigated the preponderant role of PR-10 in plant defense against biotic stresses; however, little is known about the mechanisms of action of these proteins. This is the first systematic review conducted to gather information on the subject and to reveal the possible mechanisms of action that PR-10 perform.

Methods: Therefore, three databases were used for the article search: PubMed, Web of Science, and Scopus. To avoid bias, a protocol with inclusion and exclusion criteria was prepared. In total, 216 articles related to the proposed objective of this study were selected.

Results: The participation of PR-10 was revealed in the plant's defense against several stressor agents such as viruses, bacteria, fungi, oomycetes, nematodes and insects, and studies involving fungi and bacteria were predominant in the selected articles. Studies with combined techniques showed a compilation of relevant information about PR-10 in biotic stress that collaborate with the understanding of the mechanisms of action of these molecules. The up-regulation of PR-10 was predominant under different conditions of biotic stress, in addition to being more expressive in resistant varieties both at the transcriptional and translational level.

Discussion: Biological models that have been proposed reveal an intrinsic network of molecular interactions involving the modes of action of PR-10. These include hormonal pathways, transcription factors, physical interactions with effector proteins or pattern recognition receptors and other molecules involved with the plant's defense system.

Conclusion: The molecular networks involving PR-10 reveal how the plant's defense response is mediated, either to trigger susceptibility or, based on data systematized in this review, more frequently, to have plant resistance to the disease.

Keywords: defense mechanism; pathogens; signal transduction; stress; systematic review.

Figure 1

Flowchart with identification and selection of studies according to PRISMA guidelines (Page et al., 2021).

Figure 2

Bibliometric indicators of scientific knowledge production and dissemination on the SR subject of the selected articles. (A) Article distribution by journal. (B) Collaboration network between authors. (C) Collaboration network between research institutions. (D) Network of co-occurrence of words in the selected articles’ titles. (E) Collaboration network between countries. In (B, C, E), the size of the circle represents the number of article occurrences (the larger the circle, the greater the article number), the thickness of the lines represent the number of collaborations between authors, and research institutions or countries (the thicker the line, the greater the number), respectively. Colors define node clusters that have similar patterns of collaboration. In (D), the circle’s size represents the number of articles with occurrences of the term in the title (the larger the circle, the greater the occurrence). The line thickness defines the number of co-occurrences of two terms (the thicker the line, the greater the co-occurrence). Colors define clusters of terms that frequently appear together in article titles.

Figure 3

Bibliometric indicators of the selected articles. (A) Main countries that published about PR-10. (B) Main methods applied in the selected articles related to PR-10.

Figure 4

Percentage of articles showing PR-10 expression (transcriptional level) or accumulation (translational level) in plants subjected to biotic stresses. (A) Percentage total of articles (gray graph) showing up- or down- regulation of PR-10 expression in plants subjected to different stressors (inset). (B) Percentage total of articles (gray graph) showing induction or repression of PR-10 proteins in plants subjected to different stressors (inset). Some articles contained data about both up- and down- regulation, or both induction and repression of PR-10, for this reason the sum of some percentages does not add up to 100%.

Figure 5

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to fungal stress. Thin, non-dotted arrows indicate a direct PR-10 reaction. Dotted arrows indicate an indirect reaction, involving steps or molecules as yet unknown or not shown. Thick white arrows indicate the role PR-10 played (blue boxes). (+) or (-) indicates positive or negative regulation, and increase or decrease of the performed function, respectively. Red arrow indicates ROS increase. Green boxes represent molecules that regulate PR-10 expression or interact directly with it. The mustard-colored box indicates an effector. Gray boxes indicate signaling pathways involving phytohormones. Yellow-colored boxes indicate the acquired response. Open boxes indicate processes or molecules that involve the function performed by PR-10. Pink circles indicate reactions that contribute to disease resistance. The red (x) indicates the interruption of the action.

Figure 6

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to stress caused by bacteria. Thin, nondotted arrows indicate a direct PR-10 reaction. Dotted arrows indicate an indirect reaction, involving steps or molecules as yet unknown or not shown. Thick white arrows indicate the role played by PR-10 (blue boxes). (+) or (-) indicate positive or negative regulation, and increase or decrease of the performed function, respectively. Red arrow indicates ROS increase. Green boxes represent molecules that regulate PR-10 expression or interact directly with it. Gray boxes indicate signaling pathways involving phytohormones. Yellow-colored box indicates the acquired response. Open boxes indicate processes or molecules that involve the function performed by PR-10. Pink circles indicate reactions that contribute to disease resistance. Black circle indicates methyl group release.

Figure 7

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to stress caused by oomycetes. Thin, nondotted arrows indicate a direct PR-10 reaction. Dotted arrows indicate an indirect reaction, involving steps or molecules as yet unknown or not shown. Thick white arrow indicates the role played by PR-10 (blue box). (+) or (-) indicate positive or negative regulation, and increase or decrease of the performed function, respectively. Red arrow indicates ROS increase. Green boxes represent molecules that regulate PR-10 expression or interact directly with it. Gray boxes indicate signaling pathways involving phytohormones. Yellow-colored box indicates the acquired response. Open boxes indicate processes or molecules that involve the function performed by PR-10. Pink circle indicates reaction that contribute to disease resistance.

Figure 8

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to stress caused by insects. Thin, non-dotted arrows indicate a direct PR-10 reaction. (+) or (-) indicate positive or negative regulation, and increase or decrease of the performed function, respectively. Red arrow indicates ROS increase. Green boxes represent molecules that regulate PR-10 expression or interact directly with it. Gray boxes indicate signaling pathways involving phytohormones. Yellow-colored box indicates the acquired response. Open boxes indicate processes or molecules that involve the function performed by PR-10.

Figure 9

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to stress caused by nematodes. Thin, non-dotted arrows indicate a direct PR-10 reaction. Dotted arrows indicate an indirect reaction, involving steps or molecules as yet unknown or not shown. (+) indicates positive regulation and increase of the performed function. Green boxes represent molecules that regulate PR-10 expression or interact directly with it. The mustard-colored box indicates an effector. Gray boxes indicate signaling pathways involving phytohormones. Yellow-colored boxes indicate the acquired response. Pink circle indicates reaction that contribute to disease resistance.

Figure 10

Biological model of a signaling network in which PR-10 is involved in the responses of plants subjected to stress caused by viruses. Thin, non-dotted arrows indicate a direct PR-10 reaction. Dotted arrows indicate an indirect reaction, involving steps or molecules as yet unknown or not shown. (+) indicates positive regulation. Green boxes represent molecules that regulate PR-10 expression. Gray box indicates signaling pathways involving phytohormones. Yellow-colored box indicates the acquired response. Pink circles indicate reactions that contribute to disease resistance.