Produced by the International Association for the Plant Protection Sciences (IAPPS). To join IAPPS and receive the Crop Protection journal online go to: www.plantprotection.org
Volatile organic compounds (VOCs) produced by soil bacteria have been shown to exert plant pathogen biocontrol potential owing to their strong antimicrobial activity. While the impact of VOCs on soil microbial ecology is well established, their effect on plant pathogen evolution is yet poorly understood. Here we experimentally investigated how plant-pathogenic Ralstonia solanacearum bacterium adapts to VOC-mixture produced by a biocontrol Bacillus amyloliquefaciens T-5 bacterium and how these adaptations might affect its virulence. We found that VOC selection led to a clear increase in VOC-tolerance, which was accompanied with cross-tolerance to several antibiotics commonly produced by soil bacteria. The increasing VOC-tolerance led to trade-offs with R. solanacearum virulence, resulting in almost complete loss of pathogenicity in planta. At the genetic level, these phenotypic changes were associated with parallel mutations in genes encoding lipopolysaccharide O-antigen (wecA) and type-4 pilus biosynthesis (pilM), which both have been linked with outer membrane permeability to antimicrobials and plant pathogen virulence. Reverse genetic engineering revealed that both mutations were important, with pilM having a relatively larger negative effect on the virulence, while wecA having a relatively larger effect on increased antimicrobial tolerance. Together, our results suggest that microbial VOCs are important drivers of bacterial evolution and could potentially be used in biocontrol to select for less virulent pathogens via evolutionary trade-offs.
Abstract The role of rhizosphere microbiota in the resistance of tomato plant against soil-borne Fusarium wilt disease (FWD) remains unclear. Here, we showed that the FWD incidence was significantly negatively correlated with the diversity of both rhizosphere bacterial and fungal communities. Using the microbiological culturomic approach, we selected 205 unique strains to construct different synthetic communities (SynComs), which were inoculated into germ-free tomato seedlings, and their roles in suppressing FWD were monitored using omics approach. Cross-kingdom (fungi and bacteria) SynComs were most effective in suppressing FWD than those of Fungal or Bacterial SynComs alone. This effect was underpinned by a combination of molecular mechanisms related to plant immunity and microbial interactions contributed by the bacterial and fungal communities. This study provides new insight into the dynamics of microbiota in pathogen suppression and host immunity interactions. Also, the formulation and manipulation of SynComs for functional complementation constitute a beneficial strategy in controlling soil-borne disease.
Editor’s note: This is the first in a two-part series about plant diseases on Guam and Micronesia.What happened to the huge, lush, towering, 100-year-plus gagu, or ironwood trees, that commonly dotted the island’s landscape at the University of Guam, Tiyan, Windward Hills Country Club golf course and elsewhere?
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Andersen Air Force Base’s Palm Tree Golf Course won an environmental innovation award for its handling of the coconut rhinoceros beetle.
Known by its scientific name Casuarina equisetifolia, ironwood trees are tightly integrated into Guam’s environment and local culture.
It is a hardy, pioneer, salt-resistant tree that occurs on the island’s main soil types: limestone, volcanic, and coral sand. It is propagated for windbreaks, erosion control, and urban landscapes.
Because C. equisetifolia is the dominant tree species on many of the sandy beaches of the Mariana Islands, it has become an important perching tree for the white-collared kingfisher (Halcyon chloris), the Mariana fruit-dove (Ptilinopus roseicapilla), and the white fairy tern (Gygis alba), which commonly lays eggs in the trees.
It has been continually propagated since the 1600s. Due to its buoyant cones, it likely floated to Guam’s sandy beaches thousands of years ago on currents from the central Indo-Pacific coastline.From these cones, seeds were shed and grew into trees. Over time, ironwood became one of Guam’s prominent members of the halophytic (sea-salt adapted) vegetation type.Based on what we now know, Guam’s healthiest trees tend to occur in natural areas, near the coastline and in areas not prone to drought.Cocos Island and Ritidian are just a few of the places where healthy coastal stands of ironwood can still be found.
Huge, healthy ironwood trees still dominate the shoreline of Ritidian Point in northern Guam.
Courtesy of Elizabeth Hahn
Farmer seeks help
In 2002, local grower Bernard Watson contacted University of Guam professor Robert Schlub about a group of five ironwood trees in one of his windbreaks that exhibited symptoms of rapid yellowing and death. Death occurred within a few weeks of symptom onset.This was totally unexpected because the trees in question were only 10 years old.Cross-sections of these trees exhibited areas of wetwood that were dark, water-infused, and radiated from their centers. Droplets of bacterial ooze appeared inside and outside the wetwood stained areas.Also appearing on Watson’s farm in 2002 were trees with the same cross-sectional symptoms but this time it was accompanied by thinning foliage and a much slower lethal decline.
This latter condition was quickly discovered in other areas of Guam and was coined “ironwood tree decline” by Schlub and Zelalem Mersha, a former UOG post-doctoral fellow now working as a Virginia State University research and extension plant pathologist.Unraveling the cause or causes of IWTD would become a major focus of Schlub’s work at the University of Guam for the next two decades.In the course of the investigation, the Guam team would join forces with researchers from institutes in California, Georgia, Florida, Hawaii, Louisiana, South Africa, China and Australia.Many possible causes of IWTD have been eliminated by the team over the years.
Links to the disease
Age was ruled out as an IWTD contributor, when trees of varying ages began dying in areas where decline was most severe. The failure to find a correlation between the presence of beetles or nematodes (microscopic worms) ruled them out as causing IWTD.The normal appearance of tree buds and young foliage eliminated the likelihood of viruses being involved.Seeing no link between typhoon damage and decline in tree surveys in 2008 and 2009, Typhoons Paka in 1997 or Pongsona in 2002 were eliminated as causing Guam’s ‘sick’ trees.
Over time, five things were consistently linked to IWTD: The presence of termites on the side of trees. The occurrence of wood-rot fungi at the base of trees.The exposure of trees to harmful landscaping practices and the presence of bacterial ooze in tree cross-sections caused, namely the bacteria that causes wetwood and the bacteria that causes bacterial wilt.Bacterial wilt is caused by bacteria within the Ralstonia solanacearum species complex.
Trees decline in 13 years
We now know that Guam’s wilt pathogen strain is the same one that has been killing trees in China and India for decades.One of the team’s most recent projects included a resurvey of 200 trees that were part of a survey of 1,427 conducted in 2008-09. The project was funded by the McIntire-Stennis Cooperative Forestry Research Program (project GUA932, accession no. 1017908), under the U.S. Department of Agriculture’s National Institute of Food and Agriculture.The results suggest that the decline of Guam’s ironwood trees that began in 2002 is continuing to this day, and that trees with severe wilt symptoms or that are nearly dead have high bacterial wilt infection levels.From the data, it is reasonable to expect that half the trees that appear healthy today in areas of decline such as at the University of Guam campus or Fort Soledad will begin showing symptoms of decline over the next 13 years and that trees already suffering from IWTD will likely be dead or nearly dead within the same time period.
Foliage thinning is one of the ominous signs that this ironwood tree on the University of Guam campus is suffering from decline.
Courtesy of Elizabeth Hahn
How you can help
Several steps have been taken to reduce the impact of IWTD.Hundreds of trees from various countries have been planted to add new genes to Guam’s tree population through cross-pollination.Some of these trees have been used to establish new ironwood windbreaks and others have been used as replacement trees in windbreaks with high levels of decline.Professionals and the general public are now being advised to reduce lawnmower and weed-trimmer damage to roots and the base of trees as a means to reduce infection and spread of fungi and bacteria.
To reduce transmission of Ralstonia and wetwood bacterial ooze when pruning, individuals are instructed to disinfect all tools.
Huge, healthy ironwood trees still dominate the shoreline of Ritidian Point in northern Guam.
Courtesy of Elizabeth Hahn
The public is also being advised to remove severely declined trees as a means to protect nearby healthy trees.Planting healthy, young trees of different varieties or hosts is the quickest way to restore areas with high decline.
Robert L. Schlub is a plant pathology professor and extension specialist, and Elizabeth Hahn and Julia Delorm are extension associates with the Cooperative Extension Service at the University of Guam’s College of Natural and Applied Sciences.