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Sorghum 3-Deoxyanthocyanidin Flavonoids Confer Resistance against Corn Leaf Aphid

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Abstract

In this study we examined the role of sorghum flavonoids in providing resistance against corn leaf aphid (CLA) Rhopalosiphum maidis. In sorghum, accumulation of these flavonoids is regulated by a MYB transcription factor, yellow seed1 (y1). Functional y1 alleles accumulate 3-deoxyflavonoids (3-DFs) and 3—deoxyanthocyanidins (3-DAs) whereas null y1 alleles fail to accumulate these compounds. We found that significantly higher numbers of alate CLA adults colonized null y1 plants as compared to functional y1 plants. Controlled cage experiments and pairwise choice assays demonstrated that apterous aphids preferred to feed and reproduce on null y1 plants. These near-isogenic sorghum lines do not differ in their epicuticular wax content and were also devoid of any leaf trichomes. Significantly higher mortality of CLA was observed on artificial aphid diet supplemented with flavonoids obtained from functional y1 plants as compared to null y1 plants or the relevant controls. Our results demonstrate that the proximate mechanism underlying the deleterious effects on aphids is y1-regulated flavonoids which are important defense compounds against CLA.

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Acknowledgements

This work was supported by a USDA/NIFA award 2011-67009-30017, AES awards PEN04430 and PEN04613 to SC, and start up research funds from UTRGV for RK, and an Undergraduate Research Award, Penn State College of Ag. to Cullen Dixon. We thank Dr. Hari C. Sharma for his expertise and suggestions on this study, Thomas Eubanks for assisting with electron microscopy, Scott DiLoreto for greenhouse management, Scott Harkcom for tending sorghum nurseries at Penn State Agronomy farm, Dinakaran Elango with sorghum seed multiplication, and Kameron Wittmeyer for critical reading of this manuscript. We also wish to express our gratitude for annonymous reviewers for their constructive criticisms to help finalize this manuscript.

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Author notes

  1. Nadia Frock

    Present address: School of Health Sciences, Nursing Department, Chatham University, 0 Woodland Road, Pittsburgh, PA, 15232, USA

  2. Juliet Moen

    Present address: Grove City College, 100 Campus Drive, Grove City, PA, 16127, USA

  3. Rupesh R. Kariyat and Iffa Gaffoor contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of Texas Rio Grande Valley, Edinburg, TX, 78539, USA

    Rupesh R. Kariyat

  2. Plant Science Department, The Pennsylvania State University, University Park, PA, 16803, USA

    Iffa Gaffoor, Sampurna Sattar, Cullen W. Dixon, Gary A. Thompson & Surinder Chopra

  3. Department of Entomology, The Pennsylvania State University, University Park, PA, 16803, USA

    Nadia Frock & Juliet Moen

  4. Department of Environmental System Science, ETH Zurich, 8092, Zurich, Switzerland

    Consuelo M. De Moraes & Mark C. Mescher

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  1. Rupesh R. Kariyat
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Fig. S1

Effect of Flavan-4-ols on corn leaf aphid (CLA). Aphids fed on artificial diet supplemented with flavonoid compounds extracted from the developing pericarps of either Y1-rr3 seeds (green) containing flavan-4-ols or y1-ww4 seeds (purple) were observed and compared to the control treatments of either diet only (blue), or diet supplemented with 0.5% ethanol (red). The number of live aphids feeding and walking, dead aphids and live and dead nymphs were quantified 24 (A), 48 (B), and 72 (C) hr. after start of the experiment. (PNG 53 kb)

High Resolution (TIF 294 kb)

Fig. S2

Time course of effect of 3-DAs on corn leaf aphid (CLA) survival. Adult survival (A) and offspring production (B) was assessed using an artificial diet assay. Aphid and nymphs were counted up till four days and each treatment group had four biological replicates. Differences in aphid numbers between treatments were analyzed by Two way ANOVA with time and treatment as factors. Means that do not share a letter are significantly different after post hoc Tukey test at P < 0.05. (PNG 23 kb)

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Kariyat, R.R., Gaffoor, I., Sattar, S. et al. Sorghum 3-Deoxyanthocyanidin Flavonoids Confer Resistance against Corn Leaf Aphid. J Chem Ecol 45, 502–514 (2019). https://doi.org/10.1007/s10886-019-01062-8

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