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Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens

Frontiers in Microbiology

Front. Microbiol., 18 December 2020 |

Amit K. Jaiswal1, Tesfaye D. Mengiste2, James R. Myers3, Daniel S. Egel2 and Lori A. Hoagland1*
  • 1Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United States
  • 2Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, United States
  • 3Department of Horticulture, Oregon State University, Corvallis, OR, United States

Crop domestication events followed by targeted breeding practices have been pivotal for improvement of desirable traits and to adapt cultivars to local environments. Domestication also resulted in a strong reduction in genetic diversity among modern cultivars compared to their wild relatives, though the effect this could have on tripartite relationships between plants, belowground beneficial microbes and aboveground pathogens remains undetermined. We quantified plant growth performance, basal resistance and induced systemic resistance (ISR) by Trichoderma harzianum, a beneficial soil microbe against Botrytis cinerea, a necrotrophic fungus and Phytophthora infestans, a hemi-biotrophic oomycete, in 25 diverse tomato genotypes. Wild tomato related species, tomato landraces and modern commercial cultivars that were conventionally or organically bred, together, representing a domestication gradient were evaluated. Relationships between basal and ISR, plant physiological status and phenolic compounds were quantified to identify potential mechanisms. Trichoderma enhanced shoot and root biomass and ISR to both pathogens in a genotype specific manner. Moreover, improvements in plant performance in response to Trichoderma gradually decreased along the domestication gradient. Wild relatives and landraces were more responsive to Trichoderma, resulting in greater suppression of foliar pathogens than modern cultivars. Photosynthetic rate and stomatal conductance of some tomato genotypes were improved by Trichoderma treatment whereas leaf nitrogen status of the majority of tomato genotypes were not altered. There was a negative relationship between basal resistance and induced resistance for both diseases, and a positive correlation between Trichoderma-ISR to B. cinerea and enhanced total flavonoid contents. These findings suggest that domestication and breeding practices have altered plant responsiveness to beneficial soil microbes. Further studies are needed to decipher the molecular mechanisms underlying the differential promotion of plant growth and resistance among genotypes, and identify molecular markers to integrate selection for responsiveness into future breeding programs.


Tomato (Solanum lycopersicum L.) is currently the second most important vegetable crop grown in the world and its production is growing rapidly, with the total area under cultivation having doubled during the last two decades1. This important vegetable crop is also widely used as a model for investigating plant development and pest resistance mechanisms because of its relatively short reproductive cycle, availability of a fully sequenced genome, and a variety of mutants which allow investigation of individual plant traits. Tomato (Solanum spp.) originated from western South America along the Andes in Peru, Ecuador and Chile, and the Galapagos Islands (Bergougnoux, 2014). Modern tomato is thought to have been domesticated from its wild ancestors (S. pimpinellifolium and S. lycopersicum var. cerasiforme), and then selected for adaptive traits in local agronomic environments (Zhu et al., 2018). The exact site of tomato domestication is unclear, but it is thought to have occurred in Mexico or Peru (Bai and Lindhout, 2007Bergougnoux, 2014). Before the Spanish transported tomato from Mexico to Europe in the 15th century, its domestication was in a fairly advanced phase, although over the past centuries, further selection occurred at a much more intense level throughout Europe and the rest of the world (Sims, 1979). The combination of early domestication events followed by targeted breeding practices have resulted in the development of modern tomato cultivars with diverse agronomic traits including improved fruit characteristics (set, size, shape, color, firmness, shelf-life, phenolic contents) and plant growth habits (self-pruning, height, and earliness) (Bai and Lindhout, 2007Causse et al., 2007Bauchet and Causse, 2012). However, these practices have also resulted in a strong reduction in the genetic diversity of modern cultivars compared to their wild relatives. For instance, basal defenses against pests have been weakened because of selection for higher yield and fruit quality may have come at the expense of defense traits (Chen et al., 2015).

Tomato plants are susceptible to over 200 pests and diseases caused by pathogenic fungi, bacteria, viruses and nematodes (Lukyanenko, 1991). Over evolutionary time, plants have developed constitutive and induced defense mechanisms to defend against these pathogens (War et al., 2012Boots and Best, 2018). Constitutive (preformed) defenses include mechanical barriers (such as cell walls, waxy epidermal cuticles, stomatal structure, trichomes, and bark), and biochemical barriers (primary and secondary metabolites) that are always present in the plant. In contrast, induced defense mechanisms, or induced resistance (IR) responses, are activated in response to pathogen attack, and thus are less energetically expensive. IR is initiated by a specific stimulus, which allows plants to limit subsequent pest challenges (Vallad and Goodman, 2004). Among IR responses that are activated against a broad range of pests and pathogens are systemic acquired resistance (SAR), and induced systemic resistance (ISR). SAR, which is generally initiated by a hypersensitive reaction resulting from a local infection, is thought to be mediated by salicylic acid and involve the synthesis of PR (pathogenesis-related) proteins. SAR can be triggered by both biological and chemical elicitors [such as 2,6-dichloroisoniciotinic acid (INA), acibenzolar-S-methyl (BTH), and β-aminobutyric acid (BABA)] (Vallad and Goodman, 2004Vlot et al., 2009). In contrast, ISR is generally activated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF) and is thought to be mediated by the phytohormones jasmonic acid and ethylene (Vallad and Goodman, 2004Pieterse et al., 2014). Consequently, the plant microbiome is now widely regarded as a key determinant of plant health, and interest in identifying strategies that can enrich beneficial microbial communities to increase plant productivity and suppress diseases is growing rapidly. Trichoderma spp. are one group of microbes that have received much attention for their potential to stimulate plant growth and ISR. Trichoderma spp., which are members of the Ascomycetes fungi and opportunistic symbionts, have been widely used as biopesticides and biofertilizers in agricultural fields. Currently, more than 60% of all registered biopesticides contain a single Trichoderma isolate or mixture of Trichoderma species (Lopez-Bucio et al., 2015). The positive influence of Trichoderma on host plants could be related to several mechanisms, including ISR, but this is still not well understood.

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