Origin of agricultural plant pathogens: Diversity and pathogenicity of Rhizoctonia fungi associated with native prairie grasses in the Sandhills of Nebraska.

Srikanth Kodati,Jerry D Volesky,Gary Y Yuen,Anthony O Adesemoye,Sydney E Everhart,Vijai Gupta

doi:10.1371/journal.pone.0249335

Abstract

The Sandhills of Nebraska is a complex ecosystem, covering 50,000 km2 in central and western Nebraska and predominantly of virgin grassland. Grasslands are the most widespread vegetation in the U.S. and once dominated regions are currently cultivated croplands, so it stands to reason that some of the current plant pathogens of cultivated crops originated from grasslands, particularly soilborne plant pathogens. The anamorphic genus Rhizoctonia includes genetically diverse organisms that are known to be necrotrophic fungal pathogens, saprophytes, mycorrhiza of orchids, and biocontrol agents. This study aimed to evaluate the diversity of Rhizoctonia spp. on four native grasses in the Sandhills of Nebraska and determine pathogenicity to native grasses and soybean. In 2016 and 2017, a total of 84 samples were collected from 11 sites in the Sandhills, located in eight counties of Nebraska. The samples included soil and symptomatic roots from the four dominant native grasses: sand bluestem, little bluestem, prairie sandreed, and needle-and-thread. Obtained were 17 Rhizoctonia-like isolates identified, including five isolates of binucleate Rhizoctonia AG-F; two isolates each from binucleate Rhizoctonia AG-B, AG-C, and AG-K, Rhizoctonia solani AGs: AG-3, and AG-4; one isolate of binucleate Rhizoctonia AG-L, and one isolate of R. zeae. Disease severity was assessed for representative isolates of each AG in a greenhouse assay using sand bluestem, needle-and-thread, and soybean; prairie sandreed and little bluestem were unable to germinate under artificial conditions. On native grasses, all but two isolates were either mildly aggressive (causing 5-21% disease severity) or aggressive (21-35% disease severity). Among those, three isolates were cross-pathogenic on soybean, with R. solani AG-4 shown to be highly aggressive (86% disease severity). Thus, it is presumed that Rhizoctonia spp. are native to the sandhills grasslands and an emerging pathogen of crops cultivated may have survived in the soil and originate from grasslands.

Highlights

Natural ecosystems, such as grasslands, contain a higher level of genetic and environmental heterogeneity compared to the agroecosystems comprised of one or a few plant species with extreme genetic uniformity [1]
In 2017, 10 of the 11 isolates were collected from the soil, one isolate was collected from soil of both needle-and-thread and sand bluestem that were collected from five locations, and the other one isolate, R. zeae was isolated from the roots of a needle-and-thread grass plant
It was not surprising that Rhizoctonia spp. would be isolated at such low frequency compared to agricultural fields that typically yield approximately two isolates per five samples [37]

Summary

Introduction

Natural ecosystems, such as grasslands, contain a higher level of genetic and environmental heterogeneity compared to the agroecosystems comprised of one or a few plant species with extreme genetic uniformity [1]. It would be expected to have a high diversity of microorganisms associated with those plants in natural ecosystems. Conversion to agricultural croplands represents a dramatic form of natural ecosystem change. This can lead to selection for and emergence of plant pathogens that possess pathogenicity, the ability to cause disease, on cultivated crop plants. In terms of plant pathogens, it is expected that the high diversity of plant species in a natural ecosystem favors low virulence, generalist pathogens that can infect many host plants [2]. It is expected that this bottleneck process would select for pathogens of the crop host plant and, over time, will select for more virulent/ specialized pathogens in that ecosystem [5]. The ability of the pathogen to survive and acclimatize to the new agroecosystem from the natural ecosystem, is highly dependent on its evolutionary potential and life history traits [6]

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