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Membrane Depolarization and Apoptosis-Like Cell Death in an Alkaline Environment in the Rice Pathogen Burkholderia glumae

ABSTRACT: The rice pathogen Burkholderia glumae uses amino acids as a principal carbon source and thus produces ammonia in amino acid-rich culture medium such as Luria–Bertani (LB) broth. To counteract ammonia-mediated environmental alkaline toxicity, the bacterium produces a public good, oxalate, in a quorum sensing (QS)-dependent manner. QS mutants of B. glumae experience alkaline toxicity and may undergo cell death at the stationary phase when grown in LB medium. Here, we show that the cell-death processes of QS mutants due to alkaline environmental conditions are similar to the apoptosis-like cell death reported in other bacteria. Staining QS mutants with bis-(1,3-dibutylbarbituric acid)-trimethine oxonol revealed membrane depolarization. CellROX™ staining showed excessive generation of reactive oxygen species (ROS) in QS mutants. The expression of genes encoding HNH endonuclease (BGLU_1G15690), oligoribonuclease (BGLU_1G09120), ribonuclease E (BGLU_1G09400), and Hu-beta (BGLU_1G13530) was significantly elevated in QS mutants compared to that in wild-type BGR1, consistent with the degradation of cellular materials as observed under transmission electron microscopy (TEM). A homeostatic neutral pH was not attainable by QS mutants grown in LB broth or by wild-type BGR1 grown in an artificially amended alkaline environment. At an artificially adjusted alkaline pH, wild-type BGR1 underwent apoptosis-like cell death similar to that observed in QS mutants. These results show that environmental alkaline stress interferes with homeostatic neutral cellular pH, induces membrane depolarization, and causes apoptosis-like cell death in B. glumae.

SUBMITTER: Nam Y

PROVIDER: S-EPMC8546246 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Bacterial panicle blight caused by the bacterium Burkholderia glumae is an emerging disease of rice in the United States. Not much is known about this disease, the disease cycle or any source of disease resistance. To understand the interaction between rice and Burkholderia glumae, we used transcriptomics via next-generation sequencing (RNA-Seq) and bioinformatics to identify differentially expressed transcripts between resistant and susceptible interactions and formulate a model for rice resistance to the disease. RESULTS: Using inoculated young seedlings as sample tissues, we identified unique transcripts involved with resistance to bacterial panicle blight, including a PIF-like ORF1 and verified differential expression of some selected genes using qRT-PCR. These transcripts, which include resistance genes of the NBS-LRR type, kinases, transcription factors, transporters and expressed proteins with functions that are not known, have not been reported in other pathosystems including rice blast or bacterial blight. Further, functional annotation analysis reveals enrichment of defense response and programmed cell death (biological processes); ATP and protein binding (molecular functions); and mitochondrion-related (cell component) transcripts in the resistant interaction. CONCLUSION: Taken together, we formulated a model for rice resistance to bacterial panicle blight that involves an activation of previously unknown resistance genes and their activation partners upon challenge with B. glumae. Other interesting findings are that 1) though these resistance transcripts were up-regulated upon inoculation in the resistant interaction, some of them were already expressed in the water-inoculated control from the resistant genotype, but not in the water- and bacterium-inoculated samples from the susceptible genotype; 2) rice may have co-opted an ORF that was previously a part of a transposable element to aid in the resistance mechanism; and 3) resistance may have existed immediately prior to rice domestication.

Project description:Bacterial Panicle Blight (BPB), caused by Burkholderia glumae, is a bacterial disease in rice (Oryza sativa) that reduces rice yield and quality for producers and consequently creates higher market prices for consumers. BPB is caused by the simultaneous occurrence of high daily minimum temperatures (~22°C) and relative humidity (~77%), which may increase under the current scenario of global warming. This study hypothesized that the economic damage from warming may cause an increase in economic losses, though at a decreasing rate per degree. Thus, this study estimates the yield losses associated with BPB occurrences at the county level in the Mid-South United States (US) for annual rice production in 2003-2013 and under +1-3°C warming scenarios using daily weather information with appropriate thresholds. From the estimated losses, the total production potential of a BPB-resistant rice was quantified using a spatial equilibrium trade model to further estimate market welfare changes with the counterfactual scenario that all US county-level rice production were BPB resistant. Results from the study indicate that the alleviation of BPB would represent a $69 million USD increase in consumer surplus in the US and a concomitant increase in rice production that would feed an additional 1.46 million people annually assuming a global average consumption of 54 Kg per person. Under the 1°C warming scenario, BPB occurrences and production losses would cause price increases for rice and subsequently result in a $112 million USD annual decrease in consumer surplus in the US and a loss of production equivalent to feeding 2.17 million people. Under a 3°C warming scenario, production losses due to BPB cause an annual reduction of $204 million USD in consumer surplus in the US, and a loss in production sufficient to feed 3.98 million people a year. As global warming intensifies, BPB could become a more common and formidable rice disease to combat, and breeding for BPB resistance would be the primary line-of-defense as currently no effective chemical options are available. The results of this study inform agriculturalists, policymakers, and economists about the value of BPB-resistance in the international rice market and also help support efforts to focus future breeding toward climate change impact resilience.

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Membrane Depolarization and Apoptosis-Like Cell Death in an Alkaline Environment in the Rice Pathogen Burkholderia glumae

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