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Interplay of phytohormones facilitate sorghum tolerance to aphids

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Interactions among phytohormones are essential for providing tolerance of sorghum plants to aphids.

Abstract

Plant’s encounter with insect herbivores trigger defense signaling networks that fine-tune plant resistance to insect pests. Although it is well established that phytohormones contribute to antixenotic- and antibiotic-mediated resistance to insect pests, their role in conditioning plant tolerance, the most durable and promising category of host plant resistance, is largely unknown. Here, we screened a panel of sorghum (Sorghum bicolor) inbred lines to identify and characterize sorghum tolerance to sugarcane aphids (SCA; Melanaphis sacchari Zehntner), a relatively new and devastating pest of sorghum in the United States. Our results suggest that the sorghum genotype SC35, the aphid-tolerant line identified among the sorghum genotypes, displayed minimal plant biomass loss and a robust photosynthetic machinery, despite supporting higher aphid population. Phytohormone analysis revealed significantly higher basal levels of 12-oxo-phytodienoic acid, a precursor in the jasmonic acid biosynthesis pathway, in the sorghum SCA-tolerant SC35 plants. Salicylic acid accumulation appeared as a generalized plant response to aphids in sorghum plants, however, SCA feeding-induced salicylic acid levels were unaltered in the sorghum tolerant genotype. Conversely, basal levels of abscisic acid and aphid feeding-induced cytokinins were accumulated in the SCA-tolerant sorghum genotype. Our findings imply that the aphid-tolerant sorghum genotype tightly controls the relationship among phytohormones, as well as provide significant insights into the underlying mechanisms that contribute to plant tolerance to sap-sucking aphids.

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Acknowledgements

We would like to acknowledge Manny Saluja and John Toy for help with LI-COR data measurements and seed production, respectively. We also thank Harkamal Walia and Tala Awada for providing access to LI-COR instrument, Emily Robinson with statistical analysis, and the Proteomic and Metabolomics Facility (Center for Biotechnology at the University of Nebraska-Lincoln) for the LC–MS assay and quantification of plant hormones.

Funding

Work in the Louis laboratory was supported by funds from US National Science Foundation CAREER grant IOS-1845588 and USDA-ARS (58-3042-6-070). This work was partially supported by USDA-ARS CRIS projects 3042-21000-034-00-D (GS) and 3042-21220-033-00-D (SES). E.A. was partly supported by Undergraduate Creative Activity and Research (UCARE) and Agricultural Research Division (ARD) Undergraduate Student Research funds from the University of Nebraska-Lincoln.

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SG and JL conceived and designed the research; SG and EA performed the research; GS and SES contributed reagents, methods development and provided guidance on experiments; SG and JL wrote the paper. All authors reviewed and edited the manuscript.

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Correspondence to Joe Louis.

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Supplementary file1 (PDF 398 kb)

Supp. Fig. S1 Total number of sugarcane aphids recovered seven days after aphid infestation of two-week-old sorghum RTx430, SC35, and SC1345 plants that were initially infested with 10 adult apterous aphids per plant.

Supp. Fig. S2 Percent plant biomass loss for each sorghum NAM founder line after 14 days of sugarcane aphid (SCA) infestation of two-week-old sorghum plants that were initially infested with 10 adult apterous aphids per plant.

Supp. Fig. S3 (A) Loading plot of principal components 1 and 2 from the principal component analysis (PCA) of data collected from tolerance experiment on sorghum NAM founder lines after 14 days of SCA infestation. The loading data depicts the unrotated loading matrix between the variables and the components. Uninfested plants of similar age were used to calculate changes in plant growth upon aphid infestation. (B) Loading data of the PCA which indicates the effects of components on different variables.

Table S1 Total number of sugarcane aphids recovered 14 days after aphid infestation of two-week-old sorghum plants that were initially infested with 10 adult apterous aphids per plant.

Table S2 Plant growth parameters of sorghum genotypes with and without sugarcane aphid infestation for 14 days.

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Grover, S., Agpawa, E., Sarath, G. et al. Interplay of phytohormones facilitate sorghum tolerance to aphids. Plant Mol Biol 109, 639–650 (2022). https://doi.org/10.1007/s11103-020-01083-y

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  • DOI: https://doi.org/10.1007/s11103-020-01083-y

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