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. 2019 Nov 19;116(47):23390-23397.
doi: 10.1073/pnas.1915396116. Epub 2019 Nov 11.

Challenging battles of plants with phloem-feeding insects and prokaryotic pathogens

Yanjuan Jiang  1   2   3   4 , Chuan-Xi Zhang  5 , Rongzhi Chen  6 , Sheng Yang He  7   4   8   9
Affiliations

Challenging battles of plants with phloem-feeding insects and prokaryotic pathogens

Yanjuan Jiang et al. Proc Natl Acad Sci U S A. .

Abstract

For the past 4 decades, intensive molecular studies of mostly leaf mesophyll cell-infecting pathogens and chewing insects have led to compelling models of plant-pathogen and plant-insect interactions. Yet, some of the most devastating pathogens and insect pests live in or feed on the phloem, a systemic tissue belonging to the plant vascular system. Phloem tissues are difficult to study, and phloem-inhabiting pathogens are often impossible to culture, thus limiting our understanding of phloem-insect/pathogen interactions at a molecular level. In this Perspective, we highlight recent literature that reports significant advances in the understanding of phloem interactions with insects and prokaryotic pathogens and attempt to identify critical questions that need attention for future research. It is clear that study of phloem-insect/pathogen interactions represents an exciting frontier of plant science, and influx of new scientific expertise and funding is crucial to achieve faster progress in this important area of research that is integral to global food security.

Keywords: citrus greening; insect pest; plant immunity; plant pathogen; planthopper.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Phloem as a long-distance transport system and a habitat for prokaryotic pathogens and piercing-sucking insects. (A) A schematic source-to-sink translocation of metabolite and signaling molecules through the phloem, indicated by red arrows. (B) A cross section of phloem, indicating spatial relationships of various cell types. (C) A longitudinal diagram of phloem–insect/pathogen interactions. An insect is shown with its stylet piercing the plant tissue in order to reach a phloem sieve cell. The stylet often takes a long route in the intercellular spaces (apoplast) to reach the phloem. During this process, the stylet encounters defenses in the plant apoplastic space. As part of its counter defense strategy, the insect secretes a gelling saliva to form a hard sheath, which seals off plant cell leaks caused by the penetration process and provides a path to facilitate the stylet movement. When it has reached the phloem, the insect secretes watery saliva proteins (effector molecules) into phloem cells to interfere with, among other host processes, defense-associated callose deposition and protein plugging (P-proteins and forisome) at sieve plates. Insect vectors deliver prokaryotic pathogens into the sieve cells.
Fig. 2.
Fig. 2.
A schematic of plant cellular responses to phloem-feeding insects and prokaryotic pathogens. (A) In a resistant plant cell, the membrane-localized pattern recognition receptor (PRR) Bph3 and a coreceptor, BAK1, recognize insect- and pathogen-derived elicitors (e.g., PAMPs and HAMPs) to trigger pattern-triggered immunity (PTI). Some plants evolved disease resistant proteins, such as Mi-1.2, Bph9, and Bph14, to recognize specific “effectors” from insects and pathogens, resulting in the activation of effector-triggered immunity (ETI). Bph6 interacts with EXO70E1, correlated with strengthening plant cell walls against BPH feeding. EXO70E1, EXOCYST70E1; PAE9, PECTIN ACETYLESTERASE 9; SLI1, SIEVE ELEMENT-LINING CHAPERONE1. (B) In a susceptible plant cell lacking disease-resistant proteins and ETI, effectors from insects and pathogens target a variety of phloem cellular processes to facilitate pathogen multiplication and insect fecundity. Effectors from insects and pathogens are shown in orange color, and the plant targets are shown in green and yellow colors. NLRs, nucleotide-binding, leucine-rich repeat proteins; CLas, Ca. Liberibacter asiaticus; SDE1, Sec-delivered effector 1; PLCPs, papain-like cysteine proteases; SAP11, secretes AY-WB protein 11; TCPs, TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR; JA, jasmonic acid; SAP54, secreted AY-WB protein54; PHYL1, phytoplasma-secreted protein 1; MTFs, MADS domain transcription factors; TENGU, tengu-su inducer; ARF6/8, AUXIN RESPONSIVE FACTOR 6/8; Mp1, saliva protein 1 of M. persicae; VPS52, Vacuolar Protein Sorting Associated Protein 52; Me10, saliva protein 10 of M. euphorbiae; TFT7, tomato 14–3-3 isoform 7; NcSP84, 84-kDa calcium-binding effector protein of N. cincticeps; BPH, brown plant hopper (N. lugens); NlSEF1, an EF-hand calcium-binding motif of N. lugens; Ca2+, calcium; Bt56, a whitefly B. tabaci salivary protein; NTH202, a tobacco class II KNOTTED 1-like homeobox (KNOX) transcription factor.
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