Enhancing systemic resistance in faba bean (Vicia faba L.) to Bean yellow mosaic virus via soil application and foliar spray of nitrogen-fixing Rhizobium leguminosarum bv. viciae strain 33504-Alex1

Ahmed Abdelkhalek; Hamada El-Gendi; Abdulaziz A Al-Askar; Viviana Maresca; Hassan Moawad; Mohsen M Elsharkawy; Hosny A Younes; Said I Behiry

doi:10.3389/fpls.2022.933498

Enhancing systemic resistance in faba bean (Vicia faba L.) to Bean yellow mosaic virus via soil application and foliar spray of nitrogen-fixing Rhizobium leguminosarum bv. viciae strain 33504-Alex1

Front Plant Sci. 2022 Aug 2:13:933498. doi: 10.3389/fpls.2022.933498. eCollection 2022.

Authors

Ahmed Abdelkhalek¹, Hamada El-Gendi², Abdulaziz A Al-Askar³, Viviana Maresca⁴, Hassan Moawad⁵, Mohsen M Elsharkawy⁶, Hosny A Younes⁷, Said I Behiry⁷

Affiliations

¹ Department of Plant Protection and Biomolecular Diagnosis, Arid Lands Cultivation Research Institute (ALCRI), City of Scientific Research and Technological Applications, Alexandria, Egypt.
² Department of Bioprocess Development, Genetic Engineering and Biotechnology Research Institute, City of Scientific Research and Technological Applications, Alexandria, Egypt.
³ Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia.
⁴ Department of Biology, University of Naples "Federico II", Naples, Italy.
⁵ Department of Agricultural Microbiology, National Research Centre, Cairo, Egypt.
⁶ Department of Agricultural Botany, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh, Egypt.
⁷ Department of Agricultural Botany, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria, Egypt.

Abstract

Rhizobium spp. manifests strong nitrogen fixation ability in legumes. However, their significance as biocontrol agents and antivirals has rarely been investigated. Under greenhouse conditions, the molecularly identified nitrogen-fixing plant growth-promoting rhizobacteria (PGPR), Rhizobium leguminosarum bv. viciae strain 33504-Alex1, isolated from the root nodules of faba bean plants, was tested as a soil inoculum or a foliar application to trigger faba bean plants' resistance against Bean yellow mosaic virus (BYMV) infection. Compared to the non-treated faba bean plants, the applications of 33504-Alex1 in either soil or foliar application significantly promoted growth and improved total chlorophyll content, resulting in a considerable reduction in disease incidence and severity and the inhibition index of BYMV in the treated faba bean plants. Furthermore, the protective activities of 33504-Alex1 were associated with significant reductions in non-enzymatic oxidative stress markers [hydrogen peroxide (H₂O₂) and malondialdehyde (MDA)] and remarkably increased DPPH free radical scavenging activity and total phenolic content compared to the BYMV treatment at 20 days post-inoculation. Additionally, an increase in reactive oxygen species scavenging enzymes [superoxide dismutase (SOD) and polyphenol oxidase (PPO)] and induced transcriptional levels of pathogenesis-related (PR) proteins (PR-1, PR-3, and PR-5) were observed. Of the 19 polyphenolic compounds detected in faba bean leaves by high-performance liquid chromatography (HPLC) analysis, gallic and vanillic acids were completely shut down in BYMV treatment. Interestingly, the 33504-Alex1 treatments were associated with the induction and accumulation of the most detected polyphenolic compounds. Gas chromatography-mass spectrometry (GC-MS) analysis showed hexadecanoic acid 2,3-dihydroxypropyl ester, tetraneurin-A-Diol, oleic acid, and isochiapin B are the major compounds in the ethyl acetate extract of 33504-Alex1 culture filtrate (CF), suggesting it acts as an elicitor for the induction of systemic acquired resistance (SAR) in faba bean plants. Consequently, the capacity of R. leguminosarum bv. viciae strain 33504-Alex1 to enhance plant growth and induce systemic resistance to BYMV infection will support the incorporation of 33504-Alex1 as a fertilizer and biocontrol agent and offer a new strategy for crop protection, sustainability, and environmental safety in agriculture production.

Keywords: Bean yellow mosaic virus; GC-MS; HPLC; Rhizobium leguminosarum bv. viciae; faba bean; induced systemic resistance; oxidative stress; pathogenesis-related proteins.