3.1.2 Microbes and insects induce the emission of specific
plant volatiles
Microbes and insects modulate plant volatile emission dynamics by
decreasing some VOCs and increasing others, or by inducing de
novo VOC synthesis. Plant volatiles are produced by several metabolic
pathways, including plastidic methylerythritol phosphate and cytosolic
mevalonic acid pathways (terpenoid compounds), shikimic acid pathways
(benzoid and phenylpropanoid compounds), and oxylipin pathways [green
leaf volatiles (GLVs)] (Bouwmeester, Schuurink, Bleeker & Schiestl,
2019). The emitted VOC profile is related to the plant genotype, organ,
and type of biotic/abiotic trigger. Different comparative triggers
(e.g., chewing vs. sucking/piercing, biotroph vs. necrotroph, host vs.
non-host pathogens, and saprophytic beneficial vs. parasitic pathogenic
microbes) elicit distinct bouquets of VOCs, including the quantity and
quality of each compound and its emission time course (Castelyn,
Appelgryn, Mafa, Pretorius & Visser, 2014, Klimm, Weinhold & Volf,
2020, Qawasmeh, Raman & Wheatley, 2015, Quintana-Rodriguez,
Morales-Vargas, Molina-Torres, Ádame-Alvarez, Acosta-Gallegos, Heil &
Flynn, 2015, Sharifi et al. , 2018).
VOC profiles are conventionally defined based on what triggers their
emission. They include herbivore-induced plant volatiles (HIPVs),
oviposition-induced plant volatiles, microbe-induced plant volatiles
(MIPVs), and stress-induced plant volatiles (Kessler & Heil, 2011,
Sharifi et al. , 2018). These categories normally contain all of
the above-mentioned VOC groups, but the quantity/quality and emission
time course for each compound carries specific information. Green leaf
volatiles (GLVs) are categorized as HIPVs, especially for chewing
insects, but GLVs also are emitted from microbial pathogen-infected
plants (Ameye, Allmann, Verwaeren, Smagghe, Haesaert, Schuurink &
Audenaert, 2018). Rust disease disrupts the epidermis and induces the
release of high amounts of GLVs (Jiang et al. , 2016). By
contrast, chewing insects feeding on maize root did not elicit the
emission of GLVs, and maize root did not respond to GLVs (van Doan,
Züst, Maurer, Zhang, Machado, Mateo, Ye, Schimmel, Glauser & Robert,
2020).
Plants emit VOCs in response to signaling between plants and Invaders.
Plant VOC profiles were altered by pathogen-associated molecular
patterns (PAMPs), herbivore-associated molecular patterns (HAMPs),
damage-associated molecular patterns (DAMPs), effector proteins, and
microbial volatile compounds (Figure 2) (Ameye et al. , 2018,
Bouwmeester et al. , 2019, Rybakova, Rack-Wetzlinger, Cernava,
Schaefer, Schmuck & Berg, 2017, Sharifi et al. , 2018, Wu, Qi,
Li, Tian, Gao, Wang, Ge, Yao, Ren, Wang, Liu, Kang, Ding & Xie, 2017).
These elicitors activate defense-related hormones (e.g., JA, SA, and
their cross-talk), which in turn activate metabolic pathways that
produce the main VOC groups.
HAMPs such as volicitin, caeliferins, and β-glucosidase modify the
volatile profiles in several plants (Alborn, Turlings, Jones, Stenhagen,
Loughrin & Tumlinson, 1997, Alborn, Hansen, Jones, Bennett, Tumlinson,
Schmelz & Teal, 2007, Hopke, Donath, Blechert & Boland, 1994). These
compounds can induce or suppress specific groups of volatiles to attract
or repel parasitoids to host plants. Well-adapted maize caterpillars
(Spodoptera frugiperda ) suppress HIPVs in maize, but not in
cotton (De Lange, Laplanche, Guo, Xu, Vlimant, Erb, Ton & Turlings,
2020).
In some plant pathogens, PAMPs (e.g., flg22, laminarin, and glucan) and
effector proteins (e.g., 2b) can modify plant VOCs (Chalal, Winkler,
Gourrat, Trouvelot, Adrian, Schnitzler, Jamois & Daire, 2015, Leitner,
Kaiser, Rasmussen, Driguez, Boland & Mithöfer, 2008, Sobhy, Bruce &
Turlings, 2018, Tu, Yang, Xu, Chen, Luo, Zhu, Chen & Yan, 2017,
Tungadi, Groen, Murphy, Pate, Iqbal, Bruce, Cunniffe & Carr, 2017).
PAMPs, HAMPs, and effector proteins are perceived by pattern recognition
receptors and R proteins in plants, and subsequently activate basal and
effector-triggered plant immune responses (Bonaventure, VanDoorn &
Baldwin, 2011, Glazebrook, 2005). Insertion of single R protein and its
position in the genome can significantly change the emission of
volatiles (Figure 2) (Lazebnik, Tibboel, Dicke & van Loon, 2017).
Signaling pathways (e.g., SA- and JA-dependent pathways) leading to
systemic resistance in inoculated and neighboring plants have important
roles in volatile biosynthesis (Orlovskis & Reymond, 2020, Wenig,
Ghirardo, Sales, Pabst, Breitenbach, Antritter, Weber, Lange, Lenk,
Cameron, Schnitzler & Vlot, 2019). ENHANCED DISEASE SUSCEPTIBILITY1
(EDS1) and AvrRpm1 are essential factors in systemic acquired resistance
and important regulators of VOCs synthesis in Arabidopsis (Bichlmeier,
2017). Monoterpenes such as α- and β-pinene also induce systemic
resistance through EDS1, SA INDUCTION–DEFICIENT 2 (SID2), and
NONEXPRESSOR OF PR GENES 1 (NPR1) proteins (Figure 3) (Bichlmeier,
2017). Thus, any biological and chemical modulator of plant resistance
can change the VOC profile or prime VOC release in response to stress.Pseudomonas protegens strain CHA0 did not change β-caryophyllene
emission or expression of the β-caryophyllene synthase gene, but primed
them in response to maize beetle Diabrotica balteata (Chiriboga,
Guo, Campos-Herrera, Röder, Imperiali, Keel, Maurhofer & Turlings,
2018). Bacterial pathogens Pseudomonas syringae directly induce
the emission of 1-undecanol and (Z )-3-hexenol volatiles in common
bean, which repel spider mite (Tetranychus urticae ) (Karamanoli,
Kokalas, Koveos, Junker & Farré-Armengol, 2020). Thus, signal
cross-talk during simultaneous plant infestation with herbivores and
pathogens (Eberl, Hammerbacher, Gershenzon & Unsicker, 2018, Lazebniket al. , 2017, Peñaflor & Bento, 2019) or co-infestation with two
pests (Kroes, Weldegergis, Cappai, Dicke & van Loon, 2017, Zhang,
Broekgaarden, Zheng, Snoeren, van Loon, Gols & Dicke, 2013) can
modulate VOC emissions and attract pests and their parasitoids.