Aphis spiraecola and Aphis (Toxoptera) citricidus differently manipulate plant metabolism to gain fitness in terms of population abundance or dispersal

Abstract

The response of plant cultivars to infestation by single aphid species has been widely reported, whereas the response of plants to multiple aphid species, and the mechanisms by which various aphids benefit from the induced changes, has been largely ignored. Here we analyzed the symptoms and physiological responses of sweet orange, Citrus sinensis (L.) Osbeck (Rutaceae), as affected by Aphis spiraecola Patch and Aphis (Toxoptera) citricidus (Kirkaldy) (Hemiptera: Aphididae). We further compared the feeding behavior, population abundance, and proportion of winged morph of the two aphid species when separately feeding on sweet orange. Results showed that feeding by A. spiraecola, but not A. citricidus, caused leaf curling, reduced shoot length, shoot fresh weight, and chlorophyll concentration. In addition, A. spiraecola feeding increased the concentration of essential amino acids in leaves when compared with A. citricidus and uninfested control plants. Electrical penetration graph-studies showed that A. citricidus gained faster access and acceptance of phloem, and spent more time ingesting phloem sap, than A. spiraecola. Furthermore, after 2 weeks of infestation, A. spiraecola produced more winged morphs, whereas A. citricidus achieved higher population abundance. Thus, our results indicate that the two citrus aphids utilize divergent strategies to manipulate host metabolism, and gain fitness benefits in population abundance or winged form production. The results could improve our understanding of varied adaptive strategies of co-existing insects and extend our knowledge of aphid-plant interactions.

Plant jasmonic acid mediated contrasting effects of two citrus aphid species on Diaphorina citri Kuwayama

“…For individual aphid infestation, Aphis spiraecola only enhanced the expression of one SA marker gene, whereas Aphis citricidus only decreased the expression of one JA marker gene. In a previous study, however, we showed that Aphis spiraecola significantly activated several SA and JA marker genes of host plant, while Aphis citricidus induced SA marker genes but repressed JA marker genes expression 15 . The difference in methodology (time interval between aphid removal and leaf sample collection) between these two studies may explain these different results.…”

“…The polyphagous spirea aphid, Aphis spiraecola Patch and oligophagous brown citrus aphid, Aphis ( Toxoptera ) citricidus (Kirkaldy) are two common citrus aphid species in citrus orchards, and they occur sympatrically with Diaphorina citri in many regions 14 . During an earlier investigation, we found that Aphis spiraecola and Aphis citricidus differentially induced physiological and defense responses of host plant after 2 days of infestation 15 . We speculate such difference may subsequently induce different plant‐mediated effects on Diaphorina citri .…”

“…In a previous study, however, we showed that Aphis spiraecola significantly activated several SA and JA marker genes of host plant, while Aphis citricidus induced SA marker genes but repressed JA marker genes expression. 15 The difference in methodology (time interval between aphid removal and leaf sample collection) between these two studies may explain these different results. The plant defense responses triggered by citrus aphids and Diaphorina citri are species specific, which may arise from their long-term co-evolution with host plants.…”

“…14 During an earlier investigation, we found that Aphis spiraecola and Aphis citricidus differentially induced physiological and defense responses of host plant after 2 days of infestation. 15 We speculate such difference may subsequently induce different plant-mediated effects on Diaphorina citri.…”

Saliva-Mediated Contrasting Effects of Two Citrus Aphid Species on Asian Citrus Psyllid Feeding Behavior and Plant Jasmonic Acid Pathway

“…Similar to D. citri , many citrus aphids preferentially feed and develop on young shoots and leaves. We previously reported that the citrus aphids Aphis spiraecola Patch and Aphis ( Toxoptera ) citricidus (Kirkaldy) manipulated citrus phytohormone-dependent defenses in different ways [ 25 ] and also that A. spiraecola and A. citricidus decrease and increase D. citri reproduction and feeding, respectively [ 26 ].…”