Nutrition Rather Than Phytohormone-Dependent Defense of Host Plant Mediates the Different Response of Red- and Green-Morph Pea Aphids to Nitrogen Fertilization

Nitrogen fertilization is widely known to affect plant metabolism, which subsequently influences phytophagous insects through a bottom-up effect. The interplay between plants and insects is often overlooked in studies examining the effects of nitrogen fertilization on insect performance. Here, we assessed the performance of green and red morphs of pea aphid Acyrthosiphon pisum feeding on alfalfa Medicago truncatula with and without nitrogen fertilization and examined how nitrogen fertilization and aphid infestation affect plant amino acid composition and phytohormone-dependent defenses. The results showed that nitrogen fertilization significantly enhanced the growth rate and fecundity of the green-morph aphid but only slightly increased the growth rate of the red morph. The feeding behaviors of the two morphs of aphid were similarly inhibited by nitrogen fertilization, manifested as prolonged stylet pathway duration and shortened phloem ingestion duration. With nitrogen fertilization, the green-morph-aphid-infested plant accumulated more free amino acids, particularly essential amino acids, when compared with the red-morph aphid. Furthermore, the infestation of both morphs of aphid repressed the expression of genes involved in salicylic acid-dependent defense while enhancing those involved in jasmonic acid/ethylene signaling under nitrogen fertilization. These results suggest that nitrogen fertilization and aphid infestation interact in manipulating plant metabolism, with nutritional changes playing a vital role in the aphid morph-specific growth and fecundity response to nitrogen fertilization.