Global food and fibre security threatened by current inefficiencies in fungal identification

Abstract

Fungal pathogens severely impact global food and fibre crop security. Fungal species that cause plant diseases have mostly been recognized based on their morphology. In general, morphological descriptions remain disconnected from crucially important knowledge such as mating types, host specificity, life cycle stages and population structures. The majority of current fungal species descriptions lack even the most basic genetic data that could address at least some of these issues. Such information is essential for accurate fungal identifications, to link critical metadata and to understand the real and potential impact of fungal pathogens on production and natural ecosystems. Because international trade in plant products and introduction of pathogens to new areas is likely to continue, the manner in which fungal pathogens are identified should urgently be reconsidered. The technologies that would provide appropriate information for biosecurity and quarantine already exist, yet the scientific community and the regulatory authorities are slow to embrace them. International agreements are urgently needed to enforce new guidelines for describing plant pathogenic fungi (including key DNA information), to ensure availability of relevant data and to modernize the phytosanitary systems that must deal with the risks relating to trade-associated plant pathogens.This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.

Keywords: DNA barcoding; cryptic diversity; fungal taxonomy.

Figure 1.

Parsimony phylogeny depicting the host range and geographical distribution of strawberry-associated species belonging to the Colletotrichum acutatum species complex. Strains from Fragaria are indicated in red text and the branches and micromorphology photos of the different fungal species are colour coded. The alignment is based on a subset of the six-locus alignment of Damm et al. [43], see TreeBASE (study number 12762). Anthracnose disease of strawberry is a particularly serious problem for commercial fruit production [44], which resulted in C. acutatum being listed as a regulated plant quarantine pest by the European and Mediterranean Plant Protection Organization (EPPO) and the EU Council Directive 2000/29 Annexes I and II, from which it was removed in 2009. Sources of inoculum include infected plants, weeds and other hosts [45,46], while the pathogen is also well known to survive via latent infections on strawberries [47]. To further complicate matters, Damm et al. [43] recently separated the morpho-species C. acutatum into 31 taxa, of which 21 were shown to represent novel species. Under these circumstances, it is difficult to imagine how quarantine can be applied through attempts at visual inspection for symptoms or morphological identification of species.

Figure 2.

Species of Botryosphaeriaceae associated with cankers on (a–d) Acacia, Protea, Eucalyptus and Pinus. Diseases caused by Botryosphaeriaceae mostly follow the onset of stress [7]. Many species of Botryosphaeriaceae are known to exist via localized, latent infections in their hosts, which appears to be a common characteristic of this group [7,48]. Once introduced into a new area as latent infection or endophyte on one host, they can easily move to other hosts where these otherwise ‘innocent’ endophytes become serious pathogens. Some species of Botryosphaeriaceae can remain latent for many years as localized infections deep inside woody or other tissues. Diplodia sapinea, for example, is a common global pathogen of Pinus spp., but is also well known to exist as latent infections in wood of stems, branches, twigs, seed cones and (to a limited extent) seed [–52]. It has evidently been introduced with its host multiple times around the world, which illustrates the extent to which quarantine systems have failed to halt the movement of such latent infections [49,52].

Figure 3.

Foliar diseases caused by (a,b) Pseudocercospora eumusae and P. fijiensis on Musa, (c) Dothistroma septosporum on Pinus and (d) Pseudocercospora angolensis on Citrus. The Mycosphaerellaceae comprises one of the largest families in the Phylum Ascomycota, in which some species have evolved as latent pathogens, saprophytes or symbionts. For example, D. septosporum, the causative agent of Red Band Needle Blight disease, is an important pathogen of Pinus spp. [27], which has also been isolated from asymptomatic pine needles. Species of Pseudocercospora are commonly associated with leaf spots, with some taxa such as P. angolensis on Citrus [53], and P. fijiensis, P. musicola and P. eumusae on Musa [26] being of major quarantine concern. Other than these examples, a great number of species from diverse genera in the Mycosphaerellaceae are commonly isolated as latent pathogens, occurring on a wide range of asymptomatic host plants [25].