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An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris.

Ballhorn DJ, Younginger BS, Kautz S - BMC Plant Biol. (2014)

Bottom Line: Induced aboveground plant defenses against pathogens can have negative effects on belowground microbial symbionts.The number of rhizobia nodules and the extent of AMF colonization was significantly reduced in treatment plants when compared to controls.Our results suggest that systemically induced PPO activity is functionally involved in this above-belowground interaction.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Induced aboveground plant defenses against pathogens can have negative effects on belowground microbial symbionts. While a considerable number of studies have utilized chemical elicitors to experimentally induce such defenses, there is surprisingly little evidence that actual aboveground pathogens affect root-associated microbes. We report here that an aboveground fungal pathogen of common bean (Phaseolus vulgaris) induces a defense response that inhibits both the belowground formation of root nodules elicited by rhizobia and the colonization with arbuscular mycorrhizal fungi (AMF).

Results: Foliage of plants inoculated with either rhizobia or AMF was treated with both live Colletotrichum gloeosporioides-a generalist hemibiotrophic plant pathogen-and C. gloeosporioides fragments. Polyphenol oxidase (PPO), chitinase and β-1,3-glucanase activity in leaves and roots, as well as the number of rhizobia nodules and the extent of AMF colonization, were measured after pathogen treatments. Both the live pathogen and pathogen fragments significantly increased PPO, chitinase and β-1,3-glucanase activity in the leaves, but only PPO activity was increased in roots. The number of rhizobia nodules and the extent of AMF colonization was significantly reduced in treatment plants when compared to controls.

Conclusion: We demonstrate that aboveground fungal pathogens can affect belowground mutualism with two very different types of microbial symbionts-rhizobia and AMF. Our results suggest that systemically induced PPO activity is functionally involved in this above-belowground interaction. We predict that the top-down effects we show here can drastically impact plant performance in soils with limited nutrients and water; abiotic stress conditions usually mitigated by microbial belowground mutualists.

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Related in: MedlinePlus

Preliminary quantification of root-associated microbes. After destructive harvest of plants (n =7 plants per day; n =147 plants total) root colonization with (a) rhizobia (number of nodules) and (b) percent of roots showing arbuscular mycorrhizal fungi (AMF) colonization were quantified over a time period of 21 days. Values shown are means ± SD.
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Fig1: Preliminary quantification of root-associated microbes. After destructive harvest of plants (n =7 plants per day; n =147 plants total) root colonization with (a) rhizobia (number of nodules) and (b) percent of roots showing arbuscular mycorrhizal fungi (AMF) colonization were quantified over a time period of 21 days. Values shown are means ± SD.

Mentions: Plants used for the initial evaluation of colonization rates with rhizobia and AMF (Figure 1, Additional file 1) and experimental plants (including controls) used for inoculations and pathogen treatment experiments (Figures 2, 3, 4 and 5, Additional files 2, 3, 4 and 5) belonged to different sets of plants. Plants used for preliminary colonization observations were cultivated about a month before the set of plants used in the pathogen treatments because of logistical reasons. In the preliminary colonization trials, rhizobial nodules started to develop 9 days after inoculation with an average number of 16.3 nodules per plant by day 21 (n =7 plants destructively harvested per day; 147 total) (Figure 1a). Microscopic quantification of mycorrhizal fungi (AMF) colonization showed an initial appearance of AMF structures at day 9, as well. The average percentage of roots colonized by AMF at day 21 was 27.9% (n =7 plants analyzed per day; 147 total) (Figure 1b).Figure 1


An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris.

Ballhorn DJ, Younginger BS, Kautz S - BMC Plant Biol. (2014)

Preliminary quantification of root-associated microbes. After destructive harvest of plants (n =7 plants per day; n =147 plants total) root colonization with (a) rhizobia (number of nodules) and (b) percent of roots showing arbuscular mycorrhizal fungi (AMF) colonization were quantified over a time period of 21 days. Values shown are means ± SD.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4248430&req=5

Fig1: Preliminary quantification of root-associated microbes. After destructive harvest of plants (n =7 plants per day; n =147 plants total) root colonization with (a) rhizobia (number of nodules) and (b) percent of roots showing arbuscular mycorrhizal fungi (AMF) colonization were quantified over a time period of 21 days. Values shown are means ± SD.
Mentions: Plants used for the initial evaluation of colonization rates with rhizobia and AMF (Figure 1, Additional file 1) and experimental plants (including controls) used for inoculations and pathogen treatment experiments (Figures 2, 3, 4 and 5, Additional files 2, 3, 4 and 5) belonged to different sets of plants. Plants used for preliminary colonization observations were cultivated about a month before the set of plants used in the pathogen treatments because of logistical reasons. In the preliminary colonization trials, rhizobial nodules started to develop 9 days after inoculation with an average number of 16.3 nodules per plant by day 21 (n =7 plants destructively harvested per day; 147 total) (Figure 1a). Microscopic quantification of mycorrhizal fungi (AMF) colonization showed an initial appearance of AMF structures at day 9, as well. The average percentage of roots colonized by AMF at day 21 was 27.9% (n =7 plants analyzed per day; 147 total) (Figure 1b).Figure 1

Bottom Line: Induced aboveground plant defenses against pathogens can have negative effects on belowground microbial symbionts.The number of rhizobia nodules and the extent of AMF colonization was significantly reduced in treatment plants when compared to controls.Our results suggest that systemically induced PPO activity is functionally involved in this above-belowground interaction.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Induced aboveground plant defenses against pathogens can have negative effects on belowground microbial symbionts. While a considerable number of studies have utilized chemical elicitors to experimentally induce such defenses, there is surprisingly little evidence that actual aboveground pathogens affect root-associated microbes. We report here that an aboveground fungal pathogen of common bean (Phaseolus vulgaris) induces a defense response that inhibits both the belowground formation of root nodules elicited by rhizobia and the colonization with arbuscular mycorrhizal fungi (AMF).

Results: Foliage of plants inoculated with either rhizobia or AMF was treated with both live Colletotrichum gloeosporioides-a generalist hemibiotrophic plant pathogen-and C. gloeosporioides fragments. Polyphenol oxidase (PPO), chitinase and β-1,3-glucanase activity in leaves and roots, as well as the number of rhizobia nodules and the extent of AMF colonization, were measured after pathogen treatments. Both the live pathogen and pathogen fragments significantly increased PPO, chitinase and β-1,3-glucanase activity in the leaves, but only PPO activity was increased in roots. The number of rhizobia nodules and the extent of AMF colonization was significantly reduced in treatment plants when compared to controls.

Conclusion: We demonstrate that aboveground fungal pathogens can affect belowground mutualism with two very different types of microbial symbionts-rhizobia and AMF. Our results suggest that systemically induced PPO activity is functionally involved in this above-belowground interaction. We predict that the top-down effects we show here can drastically impact plant performance in soils with limited nutrients and water; abiotic stress conditions usually mitigated by microbial belowground mutualists.

Show MeSH
Related in: MedlinePlus