Future Climate Significantly Alters Fungal Plant Pathogen Dynamics during the Early Phase of Wheat Litter Decomposition

Abstract

Returning wheat residues to the soil is a common practice in modern agricultural systems and is considered to be a sustainable practice. However, the negative contribution of these residues in the form of "residue-borne pathogens" is recognized. Here, we aimed to investigate the structure and ecological functions of fungal communities colonizing wheat residues during the early phase of decomposition in a conventional farming system. The experiment was conducted under both ambient conditions and a future climate scenario expected in 50-70 years from now. Using MiSeq Illumina sequencing of the fungal internal transcribed spacer 2 (ITS2), we found that plant pathogenic fungi dominated (~87% of the total sequences) within the wheat residue mycobiome. Destructive wheat fungal pathogens such as Fusarium graminearum, Fusarium tricinctum, and Zymoseptoria tritci were detected under ambient and future climates. Moreover, future climate enhanced the appearance of new plant pathogenic fungi in the plant residues. Our results based on the bromodeoxyuridine (BrdU) immunocapture technique demonstrated that almost all detected pathogens are active at the early stage of decomposition under both climate scenarios. In addition, future climate significantly changed both the richness patterns and the community dynamics of the total, plant pathogenic and saprotrophic fungi in wheat residues as compared with the current ambient climate. We conclude that the return of wheat residues can increase the pathogen load, and therefore have negative consequences for wheat production in the future.

Keywords: GCEF; MiSeq Illumina sequencing; climate change; fungal ITS2; litter decomposition; mycobiome; wheat straw decomposition.

Figure 1

Overview of retrieved fungal operational taxonomic units (OTUs). (A) Rarefaction curve of 30 samples at an OTU threshold of 97% sequence similarity; (B) Venn diagram showing the overlap and distribution of fungal OTUs colonizing wheat straw at three sampling time points (0, 30, and 60 days).

Figure 2

Non-metric multidimensional scaling (NMDS) ordination diagrams of the overall fungal community colonizing wheat straw residues in (A) ambient and (B) future climate treatments; The plant pathogenic community in (C) ambient and (D) future climate treatments; The saprotrophic community in (E) ambient and (F) future climate treatments. NMDS based on Jaccard dissimilarities was used to determine the compositional variation, enclosed areas in the NMDS plot are 95% confidence ellipses, stress (data distortion) values representing the difference between distances in the reduced dimension as compared to the complete multidimensional space (a commonly accepted stress value = 0.20); (G) Results of the permutational multivariate analysis of variance (NPMANOVA) test analyzing the effects of decomposition time (sampling date), climate changes, and the interaction between the two factors on the dynamics of the overall, plant pathogenic and saprotrophic fungi colonizing wheat straw residues. Significant results (p < 0.05) from NPMANOVA are indicated in bold.

Figure 3

Relative abundance of the dominant fungal taxa at (A) order, (B) family, and (C) genus level at different sampling times (0, 30, and 60 days) under ambient and future climate treatments. Asterisks indicate taxa that differ significantly under ambient and future conditions at 0 days (t-test, p < 0.05).

Figure 4

(A) Box plots showing observed OTUs at each time point (0, 30, and 60 days) under ambient and future climate treatments, supported by the results of a two-way ANOVA; (B) Stacked bar chart showing the relative abundance of predicted fungal guilds using the FUNGuild annotation tool; Box plots showing observed richness of OTUs classed as (C) plant pathogens and (D) saprotrophs; (E) Venn diagram showing the overlap and distribution of fungal OTUs classed as plant pathogens, which colonize wheat straw at the three sampling time points (0, 30, and 60 days).

Figure 5

Microbial composition of the plant pathogenic fungal community colonizing wheat straw residues. Heat tree showing the fungal community composition at three sampling time points (0, 30, and 60 days) under ambient (A) and future (B) climate treatments. Colors represent the occurrences of OTUs. Gain of new taxa colonizing wheat straw is indicated by green circles while loss of taxa is indicated by red circles. The NPMANOVA test (Figure 2G) confirmed significant dynamics of the pathogenic mycobiome under the future climate treatment.

Figure 6

Heat map of all OTUs classed as pathotrophic fungi found to colonize wheat straw residues. The OTUs corresponded to the ”species hypothesis” in the UNITE database using ≥99% similarity threshold. Three main clusters of species were found based on the occurrence of OTUs at different sampling times of wheat straw under ambient and future climate treatments. Non-active pathogens are indicated by asterisks.