Identification of resistance parameters / mechanisms of sugar beet (Beta vulgaris) to green peach aphid Myzus persicae and black bean aphid Aphis fabae
Doctoral thesis
Date of Examination:2024-11-22
Date of issue:2025-03-07
Advisor:Dr. Torsten Will
Referee:Prof. Dr. Michael Rostás
Referee:Prof. Dr. Mark Varrelmann
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Abstract
English
The infestation of two aphid species, the green peach aphid (Myzus persicae) and black bean aphid (Aphis fabae), along with the viruses they transmit, causes significant yield losses in sugar beet (Beta vulgaris). With increasingly strict regulations on pesticide use, especially the recent EU ban on neonicotinoids, and a lack of effective alternative methods, protecting sugar beet during the early growth stage has become more challenging. Therefore, there is an urgent need to explore novel resistance mechanisms and identify potential resistant sugar beet genotypes to integrate into sugar beet breeding programs. In the first part, 25 genotypes were screened by assessing the intrinsic rate of increase (rm) of both aphid species, respectively. Susceptible and resistant candidates were selected based on the lowest or highest intrinsic rate of increase. Both aphid species showed high rm on susceptible candidates G17 and G19. In contrast, G3 and G11 were defined as resistant candidates for both aphid species because the rm values of M. persicae were negative and were among the lowest in A. fabae. Electrical penetration graph (EPG) analysis of pre-selected candidates showed tissue-specific resistance to the two aphid species. M. persicae encountered difficulties in the stylet movement before reaching the sieve element, and A. fabae faced resistance at the sieve element. Furthermore, a high incidence of black deposits was observed in more than 85% of M. persicae’s stomachs regardless of sugar beet genotypes, indicating a general and strong incompatibility between sugar beet and M. persicae in an initial phase of interaction. The resistance was further validated in a whole plant assay in the greenhouse and under semi-field conditions by the introduction of Zero-inflated count model. An assumption of temporal adaptation by M. persicae during sugar beet colonization was introduced. The second part of the research investigated the formation of stomach deposits when M. persicae was transferred from other hosts to sugar beets. Two types of stomach deposits, black and white, were examined. As hypothesized based on literature, both types were identified to have a protein nature. Based upon mass spectrometry analysis, an 18.2 kDa sugar beet-specific lectin was detected as a part of the stomach deposits from M. persicae feed on sugar beets, and its presence was confirmed in sugar beet phloem sap. Additionally, a 72-hour EPG analysis showed that the black deposit formation led to enhanced xylem ingestion activities in unadapted aphids. Transcriptome analysis of unadapted and adapted M. persicae samples revealed an elevated expression of a Cath B gene encoding a cysteine protease, and its presence in the stomach was described. All the findings support the hypothesis that sugar beet lectin, which is highly conserved in B. vulgaris, is a protein strongly correlated with the formation of black and white deposits. The adaptation of subsequent M. persicae generations to sugar beet diet appears to be driven by Cath B overexpression-mediated effects. However, the mechanism of black deposit formation remains unknown due to its strong insolubility. Possible mechanisms have been discussed, but further investigation is needed. In the third part, the nature of black deposit formation was investigated with regard to genetic variability between M. persicae and beet yellow virus (BYV) infection. Analysis of different M. persicae biotypes showed that the occurrence of black deposit formation is biotype-specific, with variations among 3 M. persicae biotypes collected from Germany, Hungary, and France. The French biotype has the lowest occurrence of formation within the first 4 days of infestation. An BYV adaptability bioassay was performed by transferring either BYV-infested sugar beet-adapted or healthy sugar beet-adapted M. persicae to healthy sugar beet leaf. Results showed that M. persicae adapted to BYV-infected plants had a higher incidence of black deposit formation compared to those adapted to virus-free sugar beet. Transcriptome analysis revealed only minor differences in gene expression between these two M. persicae populations. The impact of BYV, a semi-persistently transmitted virus located in the phloem, is primarily discussed in the area of plant physiology, probably affecting the expression, folding, or transport of the previously described plant lectin, which is known to be involved in the formation of deposits. This change likely contributes to the observed reduction of black deposits on BYV-infected sugar beet plants. The work is of practical importance as it identified sugar beet genotypes with strong aphid resistant potential that can be integrated into breeding programs. Additionally, a novel sugar beet resistance mechanism for deposit formation was described, as the identified sugar beet lectin is a highly potential elicitor for black deposit formation and subsequent aphid death. The findings of Cath B deployed by M. persicae are regarded as an adaptation strategy in response to ingested sugar beet lectin and could be manipulated to intervene in the adaptation process. Taken together, these findings can be integrated into breeding programs as a crucial component of integrated pest management (IPM) strategies. Furthermore, the results obtained provide an insight into the complex interaction between sugar beet, aphid vectors, and viruses.
Keywords: Sugar beet; Aphids; Integrated pest management; Plant-aphid interaction; Resistance screening