Fungal communities associated with almond throughout crop development: Implications for aflatoxin biocontrol management in California

PLoS One. 2018 Jun 20;13(6):e0199127. doi: 10.1371/journal.pone.0199127. eCollection 2018.

Abstract

Interactions between pathogenic and nonpathogenic fungal species in the tree canopy are complex and can determine if disease will manifest in the plant and in other organisms such as honey bees. Seasonal dynamics of fungi were studied in an almond orchard in California where experimental release of the atoxigenic biopesticide Aspergillus flavus AF36 to displace toxigenic Aspergillus strains has been conducted for five years. The presence of the vegetative compatibility group (VCG) YV36, to which AF36 belongs, in the blossoms, and the honey bees that attend these blossoms, was assessed. In blossoms, A. flavus frequencies ranged from 0 to 4.5%, depending on the year of study. Frequencies of honey bees carrying A. flavus ranged from 6.5 to 10%. Only one A. flavus isolate recovered from a blossom in 2016 belonged to YV36, while members of the VCG were not detected contaminating honey bees. Exposure of pollinator honey bees to AF36 was detected to be very low. The density of several Aspergillus species was found to increase during almond hull split and throughout the final stages of maturation; this also occurred in pistachio orchards during the maturation period. Additionally, we found that AF36 effectively limited almond aflatoxin contamination in laboratory assays. This study provides knowledge and understanding of the seasonal dynamics of Aspergillus fungi and will help design aflatoxin management strategies for almond. The evidence of the low levels of VCG YV36 encountered on almond blossoms and bees during pollination and AF36's effectiveness in limiting aflatoxin contamination in almond provided additional support for the registration of AF36 with USEPA to use in almond in California.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aflatoxins / analysis*
  • Animals
  • Aspergillus flavus / isolation & purification*
  • Bees / microbiology*
  • Bees / physiology
  • California
  • Crops, Agricultural / chemistry
  • Crops, Agricultural / microbiology*
  • Crops, Agricultural / physiology
  • Feeding Behavior
  • Flowers / microbiology
  • Food Contamination / prevention & control*
  • Food Microbiology
  • Mycobiome*
  • Nuts / microbiology*
  • Pest Control, Biological*
  • Pistacia / microbiology
  • Pollination
  • Prunus dulcis / chemistry
  • Prunus dulcis / microbiology*
  • Species Specificity
  • Trees

Substances

  • Aflatoxins

Grants and funding

This work was supported by the Almond Board of California (15-AFLA1-Michailides and 16-AFLA1-Michailides (TJM); Consejo Nacional de Ciencia y Tecnologia - Mexico, Estancia postdoctoral en el extranjero, contract number 237422 (AOB); and European Union's H2020, Marie Skłodowska Curie fellowship, contract number 658579 (JM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. In addition, none of the authors are employed, have relationship as consultants, or are working in patents, product development nor marketing of products for the Almond Board of California.