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Plant-Aphid Interactions Under Elevated CO2: Some Cues from Aphid Feeding Behavior.

Sun Y, Guo H, Ge F - Front Plant Sci (2016)

Bottom Line: Aphids are phloem feeders and are considered the only feeding guild that positively responds to elevated CO2.We will describe how these elevated CO2-induced changes in defenses, nutrients, and water statusfacilitate specific stages of aphid feeding, including penetration, phloem-feeding, and xylem absorption.We conclude that a better understanding of the effects of elevated CO2 on aphids and on aphid damage to crop plants will require research on the molecular aspects of the interaction between plant and aphid but also research on aphid interactions with their intra- and inter-specific competitors and with their natural enemies.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences Beijing, China.

ABSTRACT
Although the increasing concentration of atmospheric carbon dioxide (CO2) accelerates the accumulation of carbohydrates and increases the biomass and yield of C3 crop plants, it also reduces their nitrogen concentration. The consequent changes in primary and secondary metabolites affect the palatability of host plants and the feeding of herbivorous insects. Aphids are phloem feeders and are considered the only feeding guild that positively responds to elevated CO2. In this review, we consider how elevated CO2 modifies host defenses, nutrients, and water-use efficiency by altering concentrations of the phytohormones jasmonic acid, salicylic acid, ethylene, and abscisic acid. We will describe how these elevated CO2-induced changes in defenses, nutrients, and water statusfacilitate specific stages of aphid feeding, including penetration, phloem-feeding, and xylem absorption. We conclude that a better understanding of the effects of elevated CO2 on aphids and on aphid damage to crop plants will require research on the molecular aspects of the interaction between plant and aphid but also research on aphid interactions with their intra- and inter-specific competitors and with their natural enemies.

No MeSH data available.


Related in: MedlinePlus

Potential effects of elevated CO2 on host plant, and the cascading effects on aphid feeding using Medicago truncatula-pea aphid as examples. Elevated CO2 affects aphid feeding efficiency in three ways. First, elevated CO2 modifies the phytohormone-dependent induced defenses and plant secondary metabolites derived defense. Enhancement of the salicylic acid-dependent defense pathway increased surface and epidermis resistance while the impairment of the jasmonic acid/ethylene-dependent defense pathway decreased mesophyll and phloem resistance. The changes of resistance facilitate the penetration feeding phase (the feeding phase that occurs before the stylet reaches the phloem). Second, the impairment of ethylene signaling pathway enhanced N fixation inroot, elevated CO2 tends to increase N assimilation and non-essential amino acid supple in the phloem. Furthermore, the aphid endosymbiont Buchnera could transform non-essential amino acid into essential amino acids, which increases the output of essential amino acid for aphids. Therefore, the increased amino acid supply benefits the phloem feeding of aphids. Third, elevated CO2 decreases stomatal conductance and transpiration, which increases the water potential in M. truncatula. As a result, aphid xylem feeding and osmotic pressure regulation are enhanced under elevated CO2. These three effects of elevated CO2 (alteration of host plant defenses, of amino acid supply in the phloem, and of host and aphid water status) greatly affect aphid feeding efficiency. AA, amino acid; BAK1, BRI-ASSOCIATED RECEPTOR KINASE 1; ER, epidermis resistance; ET, Ethylene; MAPK, mitogen protein kinases; JA, jasmonic acid; MR, mesophyll resistance; PR, phloem resistance; SA, Salicylic acid; SR, surface resistance; +, positively affected by elevated CO2; -, negatively affected by elevated CO2.
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Figure 1: Potential effects of elevated CO2 on host plant, and the cascading effects on aphid feeding using Medicago truncatula-pea aphid as examples. Elevated CO2 affects aphid feeding efficiency in three ways. First, elevated CO2 modifies the phytohormone-dependent induced defenses and plant secondary metabolites derived defense. Enhancement of the salicylic acid-dependent defense pathway increased surface and epidermis resistance while the impairment of the jasmonic acid/ethylene-dependent defense pathway decreased mesophyll and phloem resistance. The changes of resistance facilitate the penetration feeding phase (the feeding phase that occurs before the stylet reaches the phloem). Second, the impairment of ethylene signaling pathway enhanced N fixation inroot, elevated CO2 tends to increase N assimilation and non-essential amino acid supple in the phloem. Furthermore, the aphid endosymbiont Buchnera could transform non-essential amino acid into essential amino acids, which increases the output of essential amino acid for aphids. Therefore, the increased amino acid supply benefits the phloem feeding of aphids. Third, elevated CO2 decreases stomatal conductance and transpiration, which increases the water potential in M. truncatula. As a result, aphid xylem feeding and osmotic pressure regulation are enhanced under elevated CO2. These three effects of elevated CO2 (alteration of host plant defenses, of amino acid supply in the phloem, and of host and aphid water status) greatly affect aphid feeding efficiency. AA, amino acid; BAK1, BRI-ASSOCIATED RECEPTOR KINASE 1; ER, epidermis resistance; ET, Ethylene; MAPK, mitogen protein kinases; JA, jasmonic acid; MR, mesophyll resistance; PR, phloem resistance; SA, Salicylic acid; SR, surface resistance; +, positively affected by elevated CO2; -, negatively affected by elevated CO2.

Mentions: The ability to fix N is regulated by several hormone signaling pathways including the ET signaling pathway (Ma et al., 2002; Penmetsa et al., 2008). When the key gene Mtskl in the ET-perception pathway was mutated in M. truncatula, the nitrogenase activity was increased about two times (Penmetsa and Cook, 1997). Previous study has shown that elevated CO2 decreases the ET signaling pathway in Arabidopsis (Sun et al., 2013). The suppression of the ET signaling pathway in M. truncatula increased nodulation and N fixation ability, which thereby satisfied the increased demand for N by plants growing under elevated CO2. The down-regulation of the ET signaling pathway, however, is accompanied by decreased ET-mediated host resistance against the pea aphid (Guo et al., 2014b). This result suggested that in the M. truncatula–pea aphid system under elevated CO2, both nutritional and resistance effects would increase the fitness of the pea aphid by suppressing the ET signaling pathway (Figure 1).


Plant-Aphid Interactions Under Elevated CO2: Some Cues from Aphid Feeding Behavior.

Sun Y, Guo H, Ge F - Front Plant Sci (2016)

Potential effects of elevated CO2 on host plant, and the cascading effects on aphid feeding using Medicago truncatula-pea aphid as examples. Elevated CO2 affects aphid feeding efficiency in three ways. First, elevated CO2 modifies the phytohormone-dependent induced defenses and plant secondary metabolites derived defense. Enhancement of the salicylic acid-dependent defense pathway increased surface and epidermis resistance while the impairment of the jasmonic acid/ethylene-dependent defense pathway decreased mesophyll and phloem resistance. The changes of resistance facilitate the penetration feeding phase (the feeding phase that occurs before the stylet reaches the phloem). Second, the impairment of ethylene signaling pathway enhanced N fixation inroot, elevated CO2 tends to increase N assimilation and non-essential amino acid supple in the phloem. Furthermore, the aphid endosymbiont Buchnera could transform non-essential amino acid into essential amino acids, which increases the output of essential amino acid for aphids. Therefore, the increased amino acid supply benefits the phloem feeding of aphids. Third, elevated CO2 decreases stomatal conductance and transpiration, which increases the water potential in M. truncatula. As a result, aphid xylem feeding and osmotic pressure regulation are enhanced under elevated CO2. These three effects of elevated CO2 (alteration of host plant defenses, of amino acid supply in the phloem, and of host and aphid water status) greatly affect aphid feeding efficiency. AA, amino acid; BAK1, BRI-ASSOCIATED RECEPTOR KINASE 1; ER, epidermis resistance; ET, Ethylene; MAPK, mitogen protein kinases; JA, jasmonic acid; MR, mesophyll resistance; PR, phloem resistance; SA, Salicylic acid; SR, surface resistance; +, positively affected by elevated CO2; -, negatively affected by elevated CO2.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4829579&req=5

Figure 1: Potential effects of elevated CO2 on host plant, and the cascading effects on aphid feeding using Medicago truncatula-pea aphid as examples. Elevated CO2 affects aphid feeding efficiency in three ways. First, elevated CO2 modifies the phytohormone-dependent induced defenses and plant secondary metabolites derived defense. Enhancement of the salicylic acid-dependent defense pathway increased surface and epidermis resistance while the impairment of the jasmonic acid/ethylene-dependent defense pathway decreased mesophyll and phloem resistance. The changes of resistance facilitate the penetration feeding phase (the feeding phase that occurs before the stylet reaches the phloem). Second, the impairment of ethylene signaling pathway enhanced N fixation inroot, elevated CO2 tends to increase N assimilation and non-essential amino acid supple in the phloem. Furthermore, the aphid endosymbiont Buchnera could transform non-essential amino acid into essential amino acids, which increases the output of essential amino acid for aphids. Therefore, the increased amino acid supply benefits the phloem feeding of aphids. Third, elevated CO2 decreases stomatal conductance and transpiration, which increases the water potential in M. truncatula. As a result, aphid xylem feeding and osmotic pressure regulation are enhanced under elevated CO2. These three effects of elevated CO2 (alteration of host plant defenses, of amino acid supply in the phloem, and of host and aphid water status) greatly affect aphid feeding efficiency. AA, amino acid; BAK1, BRI-ASSOCIATED RECEPTOR KINASE 1; ER, epidermis resistance; ET, Ethylene; MAPK, mitogen protein kinases; JA, jasmonic acid; MR, mesophyll resistance; PR, phloem resistance; SA, Salicylic acid; SR, surface resistance; +, positively affected by elevated CO2; -, negatively affected by elevated CO2.
Mentions: The ability to fix N is regulated by several hormone signaling pathways including the ET signaling pathway (Ma et al., 2002; Penmetsa et al., 2008). When the key gene Mtskl in the ET-perception pathway was mutated in M. truncatula, the nitrogenase activity was increased about two times (Penmetsa and Cook, 1997). Previous study has shown that elevated CO2 decreases the ET signaling pathway in Arabidopsis (Sun et al., 2013). The suppression of the ET signaling pathway in M. truncatula increased nodulation and N fixation ability, which thereby satisfied the increased demand for N by plants growing under elevated CO2. The down-regulation of the ET signaling pathway, however, is accompanied by decreased ET-mediated host resistance against the pea aphid (Guo et al., 2014b). This result suggested that in the M. truncatula–pea aphid system under elevated CO2, both nutritional and resistance effects would increase the fitness of the pea aphid by suppressing the ET signaling pathway (Figure 1).

Bottom Line: Aphids are phloem feeders and are considered the only feeding guild that positively responds to elevated CO2.We will describe how these elevated CO2-induced changes in defenses, nutrients, and water statusfacilitate specific stages of aphid feeding, including penetration, phloem-feeding, and xylem absorption.We conclude that a better understanding of the effects of elevated CO2 on aphids and on aphid damage to crop plants will require research on the molecular aspects of the interaction between plant and aphid but also research on aphid interactions with their intra- and inter-specific competitors and with their natural enemies.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences Beijing, China.

ABSTRACT
Although the increasing concentration of atmospheric carbon dioxide (CO2) accelerates the accumulation of carbohydrates and increases the biomass and yield of C3 crop plants, it also reduces their nitrogen concentration. The consequent changes in primary and secondary metabolites affect the palatability of host plants and the feeding of herbivorous insects. Aphids are phloem feeders and are considered the only feeding guild that positively responds to elevated CO2. In this review, we consider how elevated CO2 modifies host defenses, nutrients, and water-use efficiency by altering concentrations of the phytohormones jasmonic acid, salicylic acid, ethylene, and abscisic acid. We will describe how these elevated CO2-induced changes in defenses, nutrients, and water statusfacilitate specific stages of aphid feeding, including penetration, phloem-feeding, and xylem absorption. We conclude that a better understanding of the effects of elevated CO2 on aphids and on aphid damage to crop plants will require research on the molecular aspects of the interaction between plant and aphid but also research on aphid interactions with their intra- and inter-specific competitors and with their natural enemies.

No MeSH data available.


Related in: MedlinePlus