Comparative transcriptomic and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids

Abstract

Background: Young wheat plants are continuously exposed to herbivorous insect attack. To reduce insect damage and maintain their growth, plants evolved different defense mechanisms, including the biosynthesis of deterrent compounds named benzoxazinoids, and/or trichome formation that provides physical barriers. It is unclear whether both of these mechanisms are equally critical in providing an efficient defense for wheat seedlings against aphids-an economically costly pest in cereal production.Results: In this study, we compared the transcriptome, metabolome, benzoxazinoids, and trichome density of three selected wheat genotypes, with a focus on differences related to defense mechanisms. We chose diverse wheat genotypes: two tetraploid wheat genotypes, domesticated durum 'Svevo' and wild emmer 'Zavitan,' and one hexaploid bread wheat, 'Chinese Spring.' The full transcriptomic analysis revealed a major difference between the three genotypes, while the clustering of significantly different genes suggested a higher similarity between the two domesticated wheats than between either and the wild wheat. A pathway enrichment analysis indicated that the genes associated with primary metabolism, as well as the pathways associated with defense such as phytohormones and specialized metabolites, were different between the three genotypes. Measurement of benzoxazinoid levels at the three time points (11, 15, and 18 days after germination) revealed high levels in the two domesticated genotypes, while in wild emmer wheat, they were below detection level. In contrast to the benzoxazinoid levels, the trichome density was dramatically higher in the wild emmer than in the domesticated wheat. Lastly, we tested the bird cherry-oat aphid's (Rhopalosiphum padi) performance and found that Chinese Spring is more resistant than the tetraploid genotypes. Conclusions: Our results show that benzoxazinoids play a more significant defensive role than trichomes. Differences between the abundance of defense mechanisms in the wild and domesticated plants were observed in which wild emmer possesses high physical defenses while the domesticated wheat genotypes have high chemical defenses. These findings provide new insights into the defense adaptations of wheat plants against aphids.

The combined impacts of wheat spatial position and phenology on cereal aphid abundance

“…However, these experiments were conducted during the seedling stage (2-weeks old) and under controlled growth conditions. Young wheat plants synthesize benzoxazinoids as a defense against insects (Sue, Nakamura & Nomura, 2011;Makowska, Bakera & Rakoczy-Trojanowska, 2015;Batyrshina et al, 2020), but the compounds were not detected in later developmental stages (either juvenile or mature), except for in the dry seeds (Hanhineva et al, 2011). In the metabolic analysis in the present study, we identified three flavonoids, namely 3-caffeoylquinic acid (also known as chlorogenic acid), quercetin-3-O-rutinoside (also known as rutin), and kaempferol-3-glucoside.…”

Antibiosis to Metopolophium dirhodum (Homoptera: Aphididae) in Spring Wheat and Emmer Cultivars

“…Although more resistant cultivars may not assure that the pest populations will be always kept below the economic injury levels, it at least provides a less favorable environment for the aphid pests, with respect to the population growth rate ( Atlıhan et al 2017 ). Emmer is a rich genetic resource for wheat improvement that has been extensively studied ( Nevo 2001 ) but might have weak potential to resist pests, especially during the early growth stage ( Sotherton and van Emden 1982 , Chandrasekhar et al 2018 , Batyrshina et al 2020 ; this study). We therefore advocate that great care be taken to avoid the transmission of genes responsible for suitability to aphids from emmer, as the gene source, to T. aestivum .…”

“…Husnot). Subsequent work using the same cultivars as in Chandrasekhar et al (2018) and one bread wheat cultivar revealed increased fecundity of Rhopalosiphum padi (Linnaeus) under both of the tetraploid wheat genotypes than the bread wheat, indicating that the former were more susceptible to aphids ( Batyrshina et al 2020 ). Conversely, Migui and Lamb (2004) observed partial resistance to aphid infestation, as indicated by decreased fecundity of Sitobion avenae Fabricius, in a diploid einkorn compared with tetraploid and hexaploid species of Triticum .…”

Variation Between Three Eragrostis tef Accessions in Defense Responses to Rhopalosiphum padi Aphid Infestation

“…Then, 2 cm sections were sampled from the widest part of three leaves: (i) lower leaf (a first leaf from the base), (ii) middle leaf, and (iii) upper leaf. The three leaves were dissected, bleached in 80% (v/v) ethanol, boiled at 90°C for 20 min, and washed with distilled water as previously described ( Batyrshina et al, 2020b ). For trichome visualization, leaves were mounted on microscope slides with the adaxial side facing up, covered with glass coverslips.…”

“…Many surface characteristics, including the trichomes, cuticle, epidermis, waxes, and cell walls, can modulate these interactions ( Agrawal et al, 2009 ). The leaf surface of young wheat and barley plants are covered with non-glandular trichomes, specialized epidermal hair-like structures, that might affect aphid movement and reproduction rate ( Leybourne et al, 2019 ; Batyrshina et al, 2020b ; Correa et al, 2020 ). To cope with insect attack, plants adjust their central metabolism by transiently modifying photosynthetic efficiency and remobilizing carbon and nitrogen resources ( Meihls et al, 2012 ; Appel et al, 2014 ).…”