Plant secondary metabolite and temperature determine the prevalence of Arsenophonus endosymbionts in aphid populations.

Transmission rate and role in hosts contribute to the prevalence of an endosymbiont. However, factors affecting transmission and role of facultative endosymbionts are still not well understood. Here, we illustrated that host plants and environmental temperatures affected the transmission, relative abundance and role of Arsenophonus in the cotton aphid Aphis gossypii. The transmission rate of this endosymbiont from mother aphids to offspring was relatively lower. High temperatures impeded the transmission, and infection rates declined as aphids were exposed to 30°C. Contents of amino acids and secondary metabolites were remarkably different among host plants. Aphids feeding on zucchini leaves containing a higher titre of amino acids and lower secondary metabolites harboured a relatively lower abundance of Arsenophonus. Concentrations of an amino acid and a plant secondary metabolite, cucurbitacin B, in aphid diet were not associated with Arsenophonus abundance. However, gossypol, another plant secondary metabolite, was strongly related with the abundance. Arsenophonus imparted a fitness benefit to aphids, and the benefit was dependent on host plants and gossypol concentration. In sum, plant secondary metabolite and environmental temperature affect transmission, relative abundance and role of Arsenophonus, which determine the endosymbiont prevalence in aphid populations.

Infections with Arsenophonus Facultative Endosymbionts Alter Performance of Aphids (Aphis gossypii) on an Amino-Acid-Deficient Diet.

Genetic polymorphism and endosymbiont infection are ubiquitous in aphid populations. It has been known that the obligate symbiont Buchnera provides aphids with essential amino acids which cannot be ingested from plant sap. Buchnera often coexists with facultative endosymbionts in aphids. However, it is unclear whether the facultative endosymbionts affect the aphid's amino acid requirements from diet. In this study, we found that the facultative endosymbiont status in populations of the cotton-melon aphid Aphis gossypii was associated with aphid genotype or host plant. The infection frequency of Arsenophonus in aphids living on cotton was significantly higher than that in aphids on cucumber, and cucumber leaves contained higher titers of free amino acids than cotton leaves, especially amino acids Leu, Arg, Ile, Val, and Phe. The net reproductive rates of five aphid genotypes infected with Arsenophonus were not different on the complete-amino-acid diet, but the values were significantly different among seven Arsenophonus-free aphid genotypes. Moreover, the net reproductive rates of aphids on the amino-acid-deficient diet were significantly affected by Arsenophonus infection and aphid genotype. Arsenophonus infection decreased aphid performance on the Phe-free diet but improved performance on the Leu-free diet and did not affect the performance on the Ile-free or Val-free diet. Arsenophonus infections altered aphid requirements for amino acids that were significantly different in cotton and cucumber leaves, suggesting this endosymbiont would modulate the host specialization of this aphid.IMPORTANCE The facultative endosymbiont Arsenophonus plays an important role in regulating reproduction through son killing, enemy resistance, and the dietary breadth of its insect hosts. In this study, we found Arsenophonus could alter aphid performance on the amino-acid-deficient diets. Arsenophonus infection increased aphid requirements for the amino acid Phe, but decreased requirements for the Leu. Cotton and cucumber leaves contained drastically different titers of free amino acids Phe and Leu, and aphids living on these two plants were infected with different incidences of Arsenophonus We hypothesize that host specialization or the host plant range of aphids may be mediated by Arsenophonus.

Comparative Transcriptional Analysis of the Host-Specialized Aphids Aphis gossypii (Hemiptera: Aphididae).

Host specialization is an ubiquitous character in aphid populations. Many polyphagous aphid populations usually consist of several subpopulations that have strong fidelity to a specific host or a subset of host range. Host specialization is an evolutional result of food habit of insects. However, genetic basis and molecular mechanism of host specialization are still unclear. In this study, we presented a comparative analysis on global gene expression profiles of three lineages of Aphis gossypii Glover: cotton-specialized (CO), cucurbit-specialized (CU), and CU reared on cowpea (CU-cowpea), using RNA-Seq method. More than 157 million clean reads and 38,398 different unigenes were generated from transcriptomes of these three aphid lineages. The 1,106 down- and 2,835 up-regulated genes were found between CO and CU, and 812 down- and 14,492 up-regulated genes between CU-cowpea and CU. Differentially expressed genes between CO and CU were enriched in sugar metabolism, immune system process, pathogen infection or symbiosis, and salivary secretion. Genes associated with cytochrome P450, major facilitator superfamily, and salivary effector were differentially expressed between CO and CU, which might be involved in determining host specialization. UDP-glycosyltransferases genes were sensitive to host shift. Carboxylesterases and digestion-related protease genes were related to both the host specialization and host shift of aphids. Expression levels of 22 out of 24 genes of CO and CU measured by RT-qPCR method were as similar as the results from RNA-seq method. This study provides a road map for future study on molecular mechanism of host specialization in aphids.