A transcriptomic snapshot of early molecular communication between Pasteuria penetrans and Meloidogyne incognita

Victor Phani,Rohit N. Shukla,Uma Rao,Keith G. Davies,Vishal S. Somvanshi

doi:10.1186/s12864-018-5230-8

Abstract

BackgroundSouthern root-knot nematode Meloidogyne incognita (Kofoid and White, 1919), Chitwood, 1949 is a key pest of agricultural crops. Pasteuria penetrans is a hyperparasitic bacterium capable of suppressing the nematode reproduction, and represents a typical coevolved pathogen-hyperparasite system. Attachment of Pasteuria endospores to the cuticle of second-stage nematode juveniles is the first and pivotal step in the bacterial infection. RNA-Seq was used to understand the early transcriptional response of the root-knot nematode at 8 h post Pasteuria endospore attachment.ResultsA total of 52,485 transcripts were assembled from the high quality (HQ) reads, out of which 582 transcripts were found differentially expressed in the Pasteuria endospore encumbered J2 s, of which 229 were up-regulated and 353 were down-regulated. Pasteuria infection caused a suppression of the protein synthesis machinery of the nematode. Several of the differentially expressed transcripts were putatively involved in nematode innate immunity, signaling, stress responses, endospore attachment process and post-attachment behavioral modification of the juveniles. The expression profiles of fifteen selected transcripts were validated to be true by the qRT PCR. RNAi based silencing of transcripts coding for fructose bisphosphate aldolase and glucosyl transferase caused a reduction in endospore attachment as compared to the controls, whereas, silencing of aspartic protease and ubiquitin coding transcripts resulted in higher incidence of endospore attachment on the nematode cuticle.ConclusionsHere we provide evidence of an early transcriptional response by the nematode upon infection by Pasteuria prior to root invasion. We found that adhesion of Pasteuria endospores to the cuticle induced a down-regulated protein response in the nematode. In addition, we show that fructose bisphosphate aldolase, glucosyl transferase, aspartic protease and ubiquitin coding transcripts are involved in modulating the endospore attachment on the nematode cuticle. Our results add new and significant information to the existing knowledge on early molecular interaction between M. incognita and P. penetrans.

Highlights

Southern root-knot nematode Meloidogyne incognita (Kofoid and White, 1919), Chitwood, 1949 is a key pest of agricultural crops
Transcriptome sequencing and differentially expressed genes The RNA sequencing of the Pasteuria endospore encumbered M. incognita second stage juvenile (J2) s and non-encumbered J2 s generated 32 to 39 million reads per sample (Table 2)
The silencing of transcripts coding for fructose bisphosphate aldolase (TR10010) and glucosyl transferase (TR14793) resulted in approximately six times lower endospore attachment as compared to the controls, whereas, silencing of aspartic protease (TR16177) and ubiquitin (TR10990) coding transcripts resulted in approximately three fold higher incidence of endospore attachment

Summary

Introduction

Southern root-knot nematode Meloidogyne incognita (Kofoid and White, 1919), Chitwood, 1949 is a key pest of agricultural crops. Phani et al BMC Genomics (2018) 19:850 nematodes (RKN), and represents a typical naturally coevolved pathogen – hyperparasite system [15, 86]. This is an excellent system to study the early stages of the nematode infection processes by bacterial parasites. The surface of nematode cuticle plays a decisive role in facilitating the specificity of the adhesion [27, 99] and the attachment of P. penetrans endospores to an as of yet uncharacterized cuticle receptor is the primary and arguably the most crucial step of the bacterial infection [28]. The bacterium proliferates inside the worm’s body, kills it, and converts the females into an “endospore sac” containing millions of endospores [25, 82]

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