The Adaptation Of The Diamondback Moth To Pisum Sativum Mediated By Its Detoxification Genes And Microbiota

The diamondback moth(DBM),Plutella xylostella,is suggested to have coevolved with the cruciferous plants,and its host plants include wild cruciferous plants and cultivated Brassica food crops.Recently,a DBM population was found to be able to attack and cause heavy damage to pea(Pisum sativum)in the field,demonstrating that the host range of the DBM has expanded.However,the mechanism for adaptation of the DBM to this host remains unclear.Understanding the capacity of the DBM to adapt to pea and the molecular mechanism underlying the adaptation is of great significance in uncovering the rapid evolution of the DBM and its complex relationship with plants.To answer the above scientific questions,in this study,a laboratory population feeding on radish(Raphanus sativus)for a long time was shortterm transferred or long-term adapted to pea,and the population fitness,gene expression and gut microbiota composition of short-term transferred and long-term adapted DBM populations were compared to reveal the mechanism of DBM adaptation to pea.The main results are summarized below.1.Effect of a host plant(pea)on the population fitness of the DBMThe life table data suggested that development duration of the larva and pupa of DBM were remarkably shortened with the increase of domestication generation on pea,while the longevity of male adult and female adult were significantly prolonged.Similarly,with the increase of domestication generation on pea,the intrinsic rate of increase(r),the finite increase rate(?),and the net reproduction rate(R0)of DBM's were all significantly increased,however,the population generation time(T)was remarkably shortened.The survival rate of DBM was only 9.5%when the population constantly feeding on radish was temporarily shifted to pea,while it was significantly increased to 65%after nine generation of domestication of DBM on pea.Our findings indicate that DBM can quickly adapt to pea and provide a foundation for further revealing the molecular mechanism of DBM's adaptation to pea.2.Gut microbiota mediating the adaptation of the DBM to peaThe effect of different host plants on the community of intestinal microbiota of the DBM was investigated based on 16S rDNA sequencing.We found that the dominant phylum in the gut of the DBM after long-term feeding on radish was Proteobacteria,followed by Firmicutes.When the DBM adapted to pea for five generations,the intestinal bacterial community structure of the DBM changed remarkably,and the dominant phylum was Firmicutes,followed by Proteobacteria.The population feeding on pea for five generations was subsequently transferred to the original host plant(radish)and kept for two generations.The intestinal bacterial community structure was found to have significantly changed again.The abundance of Firmicutes was remarkably reduced,while the abundance of Proteobacteria was increased nearly to the point of complete dominance in the DBM population feeding on radish over the long term,suggesting that the community structure of intestinal bacteria may be responsible for the adaptation of the DBM to different host plants.The abundance of Carnobacterium maltaromaticum was increased when the DBM was feeding on pea,while it was reduced when the DBM was feeding on radish,indicating that this strain may mediate the adaptation of the DBM to pea.Based on the gut microbial metagenome,intestinal microbiota were able to help the DBM digest food,provide the DBM with nutrients,and participate in the metabolism of toxic substances,which in turn increases the adaptive capacity of the DBM.3.Transcriptional regulation associated with adaptation to pea in the DBMA transcriptomic analysis was conducted to reveal the molecular mechanism of adaptation to pea in the DBM.The results showed that genes associated with the structural constituents of cuticle were significantly upregulated when the DBM larvae feeding on radish(a native host)were shifted to pea(a challenging host).Moreover,the genes that play a role in detoxification and response to stress were also strongly upregulated after the DBM fed on pea for eight generations.This indicated that the DBM may improve its adaptability to pea by altering its cuticle structure to prevent or reduce the entry of plant toxins and by regulating the expression of detoxification genes to reduce the damage caused by plant defenses.Additionally,when the DBM population feeding on radish for a long time was adapted to pea,most transcripts encoding digestive enzymes were significantly downregulated,indicating that digestion in the DBM may have been inhibited.4.Analysis of the genetic basis of DBM adaptation to peaIn this study,we explored the genetic basis of adaptation to pea in the DBM by bulked segregant analysis.The results suggested that QTLs regulating adaptation to pea in the DBM may be located in a specific range of 6 scaffolds.The functional annotation showed that one odor-binding protein gene,four detoxification-related genes and five digestive enzymes may be involved in regulating the adaptation of the DBM to pea host plants.Taken together,the DBM may adapt to pea by altering the composition of its microbiota,remodeling its cuticle structure,and enhancing the detoxification of plant defensive compounds.