Colletotrichum spp. from Soybean Cause Disease on Lupin and Can Induce Plant Growth-Promoting Effects

Abstract

Protein crop plants such as soybean and lupin are attracting increasing attention because of their potential use as forage, green manure, or for the production of oil and protein for human consumption. Whereas soybean production only recently gained more importance in Germany and within the whole EU in frame of protein strategies, lupin production is already well-established in Germany. The cultivation of lupins is impeded by the hemibiotrophic ascomycete Colletotrichum lupini, the causal agent of anthracnose disease. Worldwide, soybean is also a host for a variety of Colletotrichum species, but so far, this seems to not be the case in Germany. Cross-virulence between lupin- and soybean-infecting isolates is a potential threat, especially considering the overlap of possible soybean and lupin growing areas in Germany. To address this question, we systematically investigated the interaction of different Colletotrichum species isolated from soybean in Brazil on German soybean and lupin plant cultivars. Conversely, we tested the interaction of a German field isolate of C. lupini with soybean. Under controlled conditions, Colletotrichum species from soybean and lupin were able to cross-infect the other host plant with varying degrees of virulence, thus underpinning the potential risk of increased anthracnose diseases in the future. Interestingly, we observed a pronounced plant growth-promoting effect for some host-pathogen combinations, which might open the route to the use of beneficial biological agents in lupin and soybean production.

Keywords: Colletotrichum; anthracnose; commensalism; lupin; mutualism; parasitism; plant growth-promoting effect; protein crop plant; soybean.

Figure 1

Results of lesion length measurements after inoculation of soybean and lupin hypocotyls. Hypocotyls of G. max cv. Abelina (a), L. albus cv. Amiga (b), and L. angustifolius cv. Lila Baer (c) were infected with Colletotrichum-inoculated toothpick tips and lesion lengths were measured after seven days. The abbreviations Ct, Cp, Cl, and Ch represent the species C. truncatum, C. plurivorum, C. lupini, and C. higginsianum, respectively. Bars represent the mean value of two to four independent biological experiments with two plants each. The roman numerals represent the number of independent experiments. Error bars show standard deviation. Asterisks indicate a statistically significant difference in comparison with the mock control, determined by a one-way ANOVA analysis on ranks, followed by Dunn’s post hoc test (p < 0.05). In the graphs, the dashed line represents the mean value of the mock control.

Figure 2

Rating of seedling emergence and development after inoculation of soybean and lupin seeds with Colletotrichum isolates. Seeds of G. max cv. Abelina (a) and L. angustifolius cv. Lila Baer plants (b) were inoculated with different Colletotrichum species and rated one week after sowing. The abbreviations Ct, Cp, Cl, and Ch represent the species C. truncatum, C. plurivorum, C. lupini, and C. higginsianum, respectively. The following categories for rating were applied: 0—seedling not emerged; 1—seedling development arrested after emergence; 2—slower or impaired seedling development in comparison with seedlings emerging from mock-inoculated seeds; 3—seedling development like the mock; 4—faster/better development in comparison with mock. Bars represent the median value of five plants and error bars show mean absolute deviation from the median. In both graphs, the dashed line represents the median value of the mock control. The experiment was repeated once with comparable results.

Figure 3

Plant growth-promoting effect of C. plurivorum inoculation on lupin development. In an independent experiment, heights of L. angustifolius cv. Lila Baer plants after inoculation of seeds with different C. plurivorum isolates were measured five weeks after sowing (a). The plants were also scored according to a lupin-adapted BBCH development scale (b). Bars represent the mean value of at least five plants and error bars show standard deviation in case of (a). In (b), ordinal data are presented; thus, median and mean absolute deviation from the median are depicted. Statistical significance in relation to the mock inoculation was tested with a one-way ANOVA analysis followed by Dunnett’s (p < 0.05, number sign) or Holm-Sidak (p < 0.05, asterisk) post hoc test (a). In (b), the test for statistical significance was performed by a one-way ANOVA analysis on ranks, followed by Dunn’s post hoc test (p < 0.05, asterisk). In both graphs, the dashed line represents the mean value of the mock control. The experiment was repeated once with similar results.

Figure 4

Plant growth-promoting effect of Colletotrichum plurivorum in the seed inoculation assay. Comparison of plants from L. angustifolius cv. Lila Baer after treatment of seed without (a, left side) or with C. plurivorum isolate LFN0010 (a, right side) seven weeks after sowing. (b,c) Enlargements of the respective white dashed boxes in (a), indicated by black arrows. White arrows in (b) point to developing flowers. Pictures correspond to data shown in Figure 3.

Figure 5

Comparison of potential cultivated area for narrow-leafed sweet lupin and soybean in Germany. Possible areas for cultivation of narrow-leafed sweet lupin (a vertical hatching) and soybean (b, vertical hatching) based on soil–climate areas are illustrated. An overlay of (a) and (b) shows the overlap of areas (c, gray-underlaid cross-hatching). Data for maps were obtained and modified from Julius Kühn-Institut (geoportal.julius-kuehn.de, accessed 1 May 2021) under license according to German GeoNutzV and from German Federal Agency for Cartography and Geodesy (http://www.bkg.bund.de, accessed 1 May 2021) under Data license Germany—attribution—Version 2.0 (dl-de/by-2-0).