Abstract
The foliar nematode (Aphelenchoides fragariae) is a quarantined pest that infects a broad range of herbaceous and woody plants. Previous work has demonstrated its remarkable ability to survive rapid and extreme desiccation, although the specific molecular mechanisms underlying its anhydrobiotic response have not been characterized. The authors used RNA sequencing and de novo transcriptome assembly to compare patterns of gene expression between hydrated and 24-hr desiccated nematodes. In total, 2,083 and 953 genes were significantly up- and downregulated, respectively, in desiccated nematodes. Of the 100 annotated genes with the largest positive fold-changes, more than one third encoded putative detoxification-related proteins. Genes encoding enzymes of Phase I and Phase II detoxification systems were among the most strongly upregulated in the transcriptome, including 35 cytochrome p450s, 23 short chain dehydrogenase/reductases, 5 glutathione-S-transferases, and 22 UDP-glucuronosyltransferases. Genes encoding heat shock proteins, unfolded protein response enzymes, and intrinsically disordered proteins were also upregulated. Anhydrobiosis in A. fragariae appears to involve both strategies to minimize protein misfolding and aggregation, and wholesale induction of the cellular detoxification machinery. These processes may be controlled in part through the activity of forkhead transcription factors similar to Caenorhabditis elegans’ daf-16, a number of which were differentially expressed under desiccation.
Highlights
The most striking result was the wholesale upregulation of multiple genes encoding Phase I and II detoxification enzymes: numerous cytochrome p450s (CYPs), short chain dehydrogenase/reductases (SDRs), UDP-glucuronosyltransferases (UGTs), and glutathione-S-transferases (GSTs), as well as related multi-drug resistance transporters
Aphelenchoides fragariae were obtained from the Clemson University Nematode Collection where they had been cultured on Cylindrocladium sp. in potato dextrose agar (PDA, HiMedia Laboratories, India)
Among the top hundred upregulated genes were a pgp-14-like multi-drug resistance protein (MRP/PGP), an FAD-dependent monooxygenase, and multiple nuclear hormone receptors (NHRs), all of which have been implicated in the cellular detoxification program (Fig. 2; Lindblom and Dodd, 2006; Hodge and Tracy, 2010; Adhikari and Adams, 2011; Hoffmann and Partridge, 2015; Harder, 2016)
Summary
The foliar nematode, Aphelenchoides fragariae (Ritzema Bos) Christie, is a quarantined endo- and ecto-parasite that infects a broad range of herbaceous and woody host plants (Jagdale and Grewal, 2002; McCuiston et al, 2007; Kohl et al, 2010; Fu et al, 2012; Sanchez-Monge et al, 2015). Anhydrobiosis, Detoxification, Extended life span, Foliar nematode, RNA-seq, Transcriptome.
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