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Comparative Transcriptome Analysis Reveals Genetic Mechanisms of Sugarcane Aphid Resistance in Grain Sorghum.

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. However, 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.

SUBMITTER: Serba DD

PROVIDER: S-EPMC8268927 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The sugarcane aphid (Melanaphis sacchari) has emerged as a significant pest for sorghum. The use of sugarcane aphid-resistant sorghum germplasm with integrated pest management strategies appears to be an excellent solution to this problem. In this study, a resistant line (RTx2783) and a susceptible line (A/BCK60) were used to characterize the differences in plant responses to the sugarcane aphid through a series of experiments, which examined global sorghum gene expression, aphid feeding behavior and inheritance of aphid resistance. The global transcriptomic responses to sugarcane aphids in resistant and susceptible plants were identified using RNA-seq and compared to the expression profiles of uninfested plants at 5, 10, and 15 days post-infestation. The expression of genes from several functional categories were altered in aphid-infested susceptible plants, which included genes related to cell wall modification, photosynthesis and phytohormone biosynthesis. In the resistant line, only 31 genes were differentially expressed in the infested plants relative to uninfested plants over the same timecourse. However, network analysis of these transcriptomes identified a co-expression module where the expression of multiple sugar and starch associated genes were repressed in infested resistant plants at 5 and 10 days. Several nucleotide-binding-site, leucine-rich repeat (NBS-LRR) and disease resistance genes similar to aphid resistance genes identified in other plants are identified in the current study which may be involved in sugarcane aphid resistance. The electrical penetration graph (EPG) results indicated that sugarcane aphid spent approximately twice as long in non-probing phase, and approximately a quarter of time in phloem ingestion phase on the resistant and F1 plants compared to susceptible plant. Additionally, network analysis identified a phloem protein 2 gene expressed in both susceptible and resistant plants early (day 5) of infestation, which may contribute to defense against aphid feeding within sieve elements. The resistant line RTx2783 displayed both antixenosis and antibiosis modes of resistance based on EPG and choice bioassays between susceptible, resistant and F1 plants. Aphid resistance from RTx2783 segregated as a single dominant locus in the F2 generation, which will enable breeders to rapidly develop sugarcane aphid-resistant hybrids using RTx2783 as the male parent.

Project description:BackgroundSorghum grain mold is the most important disease of the crop. The disease results from simultaneous infection of the grain by multiple fungal species. Host responses to these fungi and the underlying molecular and cellular processes are poorly understood. To understand the genetic, molecular and biochemical components of grain mold resistance, transcriptome profiles of the developing grain of resistant and susceptible sorghum genotypes were studied.ResultsThe developing kernels of grain mold resistant RTx2911 and susceptible RTx430 sorghum genotypes were inoculated with a mixture of fungal pathogens mimicking the species complexity of the disease under natural infestation. Global transcriptome changes corresponding to multiple molecular and cellular processes, and biological functions including defense, secondary metabolism, and flavonoid biosynthesis were observed with differential regulation in the two genotypes. Genes encoding pattern recognition receptors (PRRs), regulators of growth and defense homeostasis, antimicrobial peptides, pathogenesis-related proteins, zein seed storage proteins, and phytoalexins showed increased expression correlating with resistance. Notably, SbLYK5 gene encoding an orthologue of chitin PRR, defensin genes SbDFN7.1 and SbDFN7.2 exhibited higher expression in the resistant genotype. The SbDFN7.1 and SbDFN7.2 genes are tightly linked and transcribed in opposite orientation with a likely common bidirectional promoter. Interestingly, increased expression of JAZ and other transcriptional repressors were observed that suggested the tight regulation of plant defense and growth. The data suggest a pathogen inducible defense system in the developing grain of sorghum that involves the chitin PRR, MAPKs, key transcription factors, downstream components regulating immune gene expression and accumulation of defense molecules. We propose a model through which the biosynthesis of 3-deoxyanthocynidin phytoalexins, defensins, PR proteins, other antimicrobial peptides, and defense suppressing proteins are regulated by a pathogen inducible defense system in the developing grain.ConclusionsThe transcriptome data from a rarely studied tissue shed light into genetic, molecular, and biochemical components of disease resistance and suggested that the developing grain shares conserved immune response mechanisms but also components uniquely enriched in the grain. Resistance was associated with increased expression of genes encoding regulatory factors, novel grain specific antimicrobial peptides including defensins and storage proteins that are potential targets for crop improvement.

Project description:BackgroundSugarcane aphid (Melanaphis sacchari) outbreaks in sorghum that were first reported in 2013 are now the most significant threat to this crop in all major sorghum production areas in the U.S. The outcomes of interactions between sugarcane aphid and sorghum and thus the severity of the outbreaks depend on sorghum genotype and potentially also on the phenology of sorghum. Mechanisms underlying these interactions are not known, however. Thus, the goal of this research was to characterize transcriptional changes in a commercially available resistant and a susceptible genotype of sorghum at 2- and 6-wk post-emergence exposed to M. sacchari herbivory. The effects of sorghum age and genotype on the daily change in aphid densities were also evaluated in separate greenhouse experiments.ResultsA higher number of diffentially expressed genes (DEGs) was recovered from the 2-wk plants exposed to aphid herbivory compared to the 6-wk plants across genotypes. Further, gene ontology and pathway analysis indicated a suite of transcriptional changes in the resistant genotype that were weak or absent in the susceptible sorghum. Specifically, the aphid-resistant genotype exposed to M. sacchari up-regulated several genes involved in defense, which was particularly evident in the 2-wk plants that showed the most robust transcriptional responses. These transcriptional changes in the younger resistant sorghum were characterized by induction of hormone-signaling pathways, pathways coding for secondary metabolites, glutathion metabolism, and plant-pathogen interaction. Furthermore, the 2-wk resistant plants appeared to compensate for the effects of oxidative stress induced by sugarcane aphid herbivory with elevated expression of genes involved in detoxification. These transcriptional responses were reflected in the aphid population growth, which was significantly faster in the susceptible and older sorghum than in the resistant and younger plants.ConclusionThis experiment provided the first insights into molecular mechanisms underlying lower population growth of M. sacchari on the resistant sorghum genotype. Further, it appears that the younger resistant sorghum was able to mount a robust defense response following aphid herbivory, which was much weaker in the older sorghum. Several pathways and specific genes provide specific clues into the mechanisms underlying host plant resistance to this invasive insect.

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Comparative Transcriptome Analysis Reveals Genetic Mechanisms of Sugarcane Aphid Resistance in Grain Sorghum.

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