The Effectiveness of Physical and Chemical Defense Responses of Wild Emmer Wheat Against Aphids Depends on Leaf Position and Genotype

Abstract

The bird cherry-oat aphid (Rhopalosiphum padi) is one of the most destructive insect pests in wheat production. To reduce aphid damage, wheat plants have evolved various chemical and physical defense mechanisms. Although these mechanisms have been frequently reported, much less is known about their effectiveness. The tetraploid wild emmer wheat (WEW; Triticum turgidum ssp. dicoccoides), one of the progenitors of domesticated wheat, possesses untapped resources from its numerous desirable traits, including insect resistance. The goal of this research was to determine the effectiveness of trichomes (physical defense) and benzoxazinoids (BXDs; chemical defense) in aphid resistance by exploiting the natural diversity of WEW. We integrated a large dataset composed of trichome density and BXD abundance across wheat genotypes, different leaf positions, conditions (constitutive and aphid-induced), and tissues (whole leaf and phloem sap). First, we evaluated aphid reproduction on 203 wheat accessions and found large variation in this trait. Then, we chose eight WEW genotypes and one domesticated durum wheat cultivar for detailed quantification of the defense mechanisms across three leaves. We discovered that these defense mechanisms are influenced by both leaf position and genotype, where aphid reproduction was the highest on leaf-1 (the oldest), and trichome density was the lowest. We compared the changes in trichome density and BXD levels upon aphid infestation and found only minor changes relative to untreated plants. This suggests that the defense mechanisms in the whole leaf are primarily anticipatory and unlikely to contribute to aphid-induced defense. Next, we quantified BXD levels in the phloem sap and detected a significant induction of two compounds upon aphid infestation. Moreover, evaluating aphid feeding patterns showed that aphids prefer to feed on the oldest leaf. These findings revealed the dynamic response at the whole leaf and phloem levels that altered aphid feeding and reproduction. Overall, they suggested that trichomes and the BXD 2,4-dihydroxy-7- methoxy-1,4-benzoxazin-3-one (DIMBOA) levels are the main factors determining aphid resistance, while trichomes are more effective than BXDs. Accessions from the WEW germplasm, rich with trichomes and BXDs, can be used as new genetic sources to improve the resistance of elite wheat cultivars.

Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (Sitobion avenae)

“…There was no correlation between the contents of DIMBOA and its glucoside compound, DIMBOA-Glc. Similar to previous studies, DIMBOA has been found in wheat tissue when β-glucosidase activity was restricted by liquid nitrogen [9,33,34]. These results indicate that DIMBOA is synthesized constitutively in wheat leaves.…”

“…Typically, benzoxazinoids are synthesized in plastids and mobilized in the phloem sap and their effect on aphids depends on their abundance in the phloem. According to previous studies, benzoxazinoid levels in the phloem sap are much lower than that of the whole wheat leaves and aphids can avoid the higher toxicity levels of benzoxazinoids in mesophyll cells by careful probing [34,46]. Moreover, aphids can avoid the negative effects of benzoxazinoids due to the detoxification system [23].…”

“…For example, the major benzox-azinoid in rye is DIBOA-Glc, whereas the most abundant benzoxazinoid in maize is DIMBOA-Glc [35,36]. In wheat plants, DIMBOA-Glc, HMBOA-Glc, HDMBOA-Glc, and DIMBOA are the most frequently identified benzoxazinoids [9,21,22,[32][33][34]. Including these four benzoxazinoids, a total of six benzoxazinoids were identified in this study and the most abundant benzoxazinoid was DIMBOA-Glc.…”

The wheat dioxygenase BX6 is involved in the formation of benzoxazinoids in planta and contributes to plant defense against insect herbivores

“…System control and data processing were performed by using the Xcalibur software (Version 4.1), Thermo Fisher, Germany). We identified the following [26,56]; ii) DIMBOA-3 Hex (2,4-dihydroxy-7methoxy-1,4-benzoxazin-3-one with three hexoses), and iii) HBOA-2 Hex (2-hydroxy-1,4benzoxazin-3-one with one hexose). Information for each BXD metabolite, including retention time, possible molecular formula, molecular weight, ion fragments in negative and positive ion modes, are presented in Supplementary Table S4.…”

“…Orthologues of the maize genes BX1-BX5 and BX8-BX9, which encode the core BXD pathway, have been identified in hexaploid bread wheat (BBAADD), tetraploid wheat (BBAA), and in the three diploid progenitors of hexaploid wheat (AA, BB, and DD subgenomes; [22,23]). Although DIMBOA-Glc and HDMBOA-Glc are abundant in wheat [24][25][26], orthologous genes of BX6 and BX7 have not been fully characterized. Very recently, Sue and coworkers described the discovery and enzymatic function of four BX6 isoforms in hexaploid T. aestivum [27].…”