Research Article: Dual RNA-seq of Xanthomonas oryzae pv. oryzicola infecting rice reveals novel insights into bacterial-plant interaction

Date Published: April 17, 2019

Publisher: Public Library of Science

Author(s): Zhou-Xiang Liao, Zhe Ni, Xin-Li Wei, Long Chen, Jian-Yuan Li, Yan-Hua Yu, Wei Jiang, Bo-Le Jiang, Yong-Qiang He, Sheng Huang, Ya-Wen He.

http://doi.org/10.1371/journal.pone.0215039

Abstract

The Gram-negative bacterium Xanthomonas oryzae pv. oryzicola (Xoc) is the causal agent of rice bacterial leaf streak (BLS), one of the most destructive diseases of rice (Oryza sativa L.) that is the important staple crop. Xoc can invade host leaves via stomata and wounds and its type three secretion system (T3SS) is pivotal to its pathogenic lifestyle. In this study, using a novel dual RNA-seq approach, we examined transcriptomes of rice and Xoc in samples inoculated with wild type Xoc GX01 and its T3SS defective strain (T3SD), to investigate the global transcriptional changes in both organisms. Compared with T3SD strain, rice inoculated with wild type Xoc GX01 resulted in significant expression changes of a series of plant defence related genes, including ones altered in plant signalling pathway, and downregulated in phenylalanine metabolism, flavonoid and momilactone biosynthesis, suggesting repression of plant defence response and reduction in both callose deposition and phytoalexin accumulation. Also, some known transcription activator-like effector (TALE) targets were induced by Xoc GX01, e.g. OsSultr3;6 which contributes to rice susceptibility. Some cell elongation related genes, including several expansin genes, were induced by GX01 too, suggesting that Xoc may exploit this pathway to weaken cell wall strength, beneficial for bacterial infection. On the other hand, compared with wild type, the T3SD strain transcriptome in planta was characterized by downregulation of ATP, protein and polysaccharide synthesis, and upregulation of antioxidation and detoxification related genes, revealing that T3SD strain faced serious starvation and oxidation stresses in planta without a functional T3SS. In addition, comparative global transcript profiles of Xoc in planta and in medium revealed an upregulation of virulence factor synthesis and secretion in planta in favour of bacterial infection. Collectively, this study provides a comprehensive representation of cross talk between the host and bacterial pathogen, revealing insights into the Xoc-rice pathogenic dynamic and reveals novel strategies exploited by this important pathogen to cause disease.

Partial Text

Oryza sativa L. (rice) is one of the world’s most important food crops and is cultivated in both tropical and temperate regions [1]. The Gram-negative bacterium Xanthomonas oryzae pv. oryzicola (Xoc) is the causative agent of bacterial leaf streak (BLS), one of the most destructive diseases of rice, which has contributed to significant yield losses (up to 30%) over the last decade [2–4]. Successful colonization by Xoc depends on its ability to adhere and adapt to the plant tissues, which serve as a frontline defence against infection. The pathogen enters rice leaves through stomata or wound sites and colonizes intercellular spaces in the mesophyll, resulting in water-soaked interveinal lesions that develop into translucent streaks[2–4]. Xoc does not invade the xylem, which is in contrast to other rice bacterial pathogens that cause bacterial blight by invading vascular tissues [2–4].

In summary, here we developed and employed a dual RNA-seq approach to examine a real-world bacterial plant disease. Combining our Xoc rice plant infection model with a robust next-generation sequencing approach we have developed a reliable real-time in situ transcriptome approach for the simultaneous monitoring of rice and Xoc gene expression levels during infection. Compared to earlier studies that used a conventional microarray to examine bacterial grown in laboratory induction medium that mimicked an in planta environment [25], our method was more reliable and resulted in better bacterial transcript coverage and sensitivity with up to 500-fold more DEGs, but also provided transcript coverage of the host plant, which benefited from both a probe-free process and a real in planta environment [26]. Furthermore, compare to previous in planta pathogenic bacteria RNA-sequencing methods that involve bacteria isolated and enriched [19], using deep sequencing can provide transcript coverage of the host plant but also avoid the potential processing issues that alter the transcriptome during the bacterial isolation[27].

 

Source:

http://doi.org/10.1371/journal.pone.0215039

 

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