Comparative transcriptome analysis reveals genetic mechanisms of sugarcane aphid resistance in grain sorghum

Authors: Serba, Desalegn; MENG, XIAOXI - University Of Nebraska; SCHNABLE, JAMES - University Of Nebraska; BASHIR, ELFADIL - Kansas State University; MICHAUD, J.P. - Kansas State University; VARA PRASAD, P.V. - Kansas State University; PERUMAL, RAMASAMY - Kansas State University

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/26/2021
Publication Date: 7/1/2021
Citation: Serba, D.D., Meng, X., Schnable, J., Bashir, E., Michaud, J., Vara Prasad, P., Perumal, R. 2021. Comparative transcriptome analysis reveals genetic mechanisms of sugarcane aphid resistance in grain sorghum. International Journal of Molecular Sciences. 22(13). https://doi.org/10.3390/ijms22137129.
DOI: https://doi.org/10.3390/ijms22137129

Interpretive Summary: The sugarcane aphid, Melanaphis sacchari (Zehntner) (Hemiptera: Aphididae) (SCA), has become a major pest of sorghum since its appearance in the USA about a decade ago. The SCA has historically infested only sugarcane. But began infesting sorghum in northeastern Mexico, Louisiana, Texas, southern Oklahoma, and eastern Mississippi in 2013. In 2014 and 2015, sorghum growers in the lower Rio Grande Valley of south Texas lost more than US $31 million due to reduced yields and the cost of insecticide applications. The aphid has now been confirmed in all 18 sorghum-growing states of the USA and only a few grain sorghum hybrids have expressed moderate resistance to the SCA. The aphid has a high reproductive rate on susceptible cultivars, can disperse far and wide with prevailing winds, and overwinter on remnant sorghum and Johnsongrass. Application of modern genomics approaches enable to understand the molecular and genetic mechanisms for resistance; and facilitates breeding for resistance cultivars in a shorter time than conventional breeding techniques. We studied the gene expression of a resistant (TAM428) and a susceptible genotype (Tx2737) using RNA sequencing to elucidate the genetic mechanisms of SCA resistance in sorghum. The results indicate that different classes of genes, including stress response genes and transcription factors that regulate the expression of multiple target genes are responsible in overcoming the physiological effects of SCA herbivory in resistant sorghum plants.

Technical Abstract: The sugarcane aphid, Melanaphis sacchari (Zehntner) (Hemiptera: Aphididae) (SCA), has become a major pest of grain sorghum since its appearance in the USA. Several grain sorghum parental lines are moderately resistant to the SCA. But, the molecular and genetic mechanisms underlying this resistance are poorly understood, which has constrained breeding for improved resistance. RNA-Seq was used to conduct transcriptomics analysis on a moderately resistant genotype (TAM428) and a susceptible genotype (Tx2737) to elucidate the molecular mechanisms underlying resistance. Differential expression analysis revealed differences in transcriptomic profile between the two genotypes at multiple time points after infestation by SCA. Six gene clusters had differential expression during SCA infestation. Gene ontology enrichment and cluster analysis of genes differentially expressed after SCA infestation revealed consistent upregulation of genes controlling protein and lipid binding, cellular catabolic processes, transcription initiation, and autophagy in the resistant genotype. Genes regulating responses to external stimuli and stress, cell communication, and transferase activities, were all upregulated in later stages of infestation. On the other hand, expression of genes controlling cell cycle and nuclear division were reduced after SCA infestation in the resistant genotype. These results indicate that different classes of genes, including stress response genes and transcription factors, are responsible for countering the physiological effects of SCA infestation in resistant sorghum plants.