Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs

Donze-Reiner, Teresa; Palmer, Nathan A.; Scully, Erin D.; Prochaska, T. J.; Koch, Kyle G.; Heng-Moss, Tiffany; Bradshaw, Jeffrey D.; Twigg, Paul; Amundsen, Keenan; Sattler, Scott E.; Sarath, Gautam

doi:10.1186/s12870-017-0998-2

Cited by 34 publications

(71 citation statements)

References 123 publications

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“…3a, b and c ). The up-regulation of genes involved in oxidative-reduction process has been reported in several plants in response to herbivory, such as in barly in response to Diuraphis noxia Kurdjumov (Hemiptera: Aphididae) [ 47 ], in switchgrass exposed to greenbug [ 48 ], in soybean at both compatible and incompatible interactions with soybean aphid [ 37 , 49 ], and in cotton in response to Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) [ 46 ]. Our outcomes corroborate these studies and suggest that oxidative responses that are elicited in the resistant genotype are may be the key components of sorghum resistance to sugarcane aphids.…”

Section: Resultsmentioning

confidence: 99%

Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum

Kiani¹,

Szczepaniec²

2018

BMC Genomics

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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.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5095-x) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum

Kiani¹,

Szczepaniec²

2018

BMC Genomics

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“…Egg deposition on leaves also induced Pip accumulation and systemic resistance dependent on both ALD1 and FMO1 (Hilfiker et al ., ), indicating that NHP functions as an inducer for this insect egg‐triggered systemic plant response. Marked accumulation of Pip also occurred in aphid‐infested soybean and switchgrass ( Panicum virgatum ) leaves, pointing to a possible role for the Pip/NHP pathway in plant–aphid interactions (Klein et al ., ; Donze‐Reiner et al ., ). In addition, roots of the model legume Lotus japonicus infected with the symbiotic rhizobium Mesorhizobium loti exhibited enhanced expression of the L. japonicus ALD1 ( LjALD1 ) gene, and silencing of LjALD1 by RNAi resulted in a reduction of the size of developing nodules (Chen et al ., ), consistent with a potential influence of Pip on nodule formation.…”

Section: Potential Involvement Of the Nhp Pathway In Other Biologicalmentioning

confidence: 97%

l‐lysine metabolism to N‐hydroxypipecolic acid: an integral immune‐activating pathway in plants

Hartmann

Zeier

2018

The Plant Journal

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l-lysine catabolic routes in plants include the saccharopine pathway to α-aminoadipate and decarboxylation of lysine to cadaverine. The current review will cover a third l-lysine metabolic pathway having a major role in plant systemic acquired resistance (SAR) to pathogen infection that was recently discovered in Arabidopsis thaliana. In this pathway, the aminotransferase AGD2-like defense response protein (ALD1) α-transaminates l-lysine and generates cyclic dehydropipecolic (DP) intermediates that are subsequently reduced to pipecolic acid (Pip) by the reductase SAR-deficient 4 (SARD4). l-pipecolic acid, which occurs ubiquitously in the plant kingdom, is further N-hydroxylated to the systemic acquired resistance (SAR)-activating metabolite N-hydroxypipecolic acid (NHP) by flavin-dependent monooxygenase1 (FMO1). N-hydroxypipecolic acid induces the expression of a set of major plant immune genes to enhance defense readiness, amplifies resistance responses, acts synergistically with the defense hormone salicylic acid, promotes the hypersensitive cell death response and primes plants for effective immune mobilization in cases of future pathogen challenge. This pathogen-inducible NHP biosynthetic pathway is activated at the transcriptional level and involves feedback amplification. Apart from FMO1, some cytochrome P450 monooxygenases involved in secondary metabolism catalyze N-hydroxylation reactions in plants. In specific taxa, pipecolic acid might also serve as a precursor in the biosynthesis of specialized natural products, leading to C-hydroxylated and otherwise modified piperidine derivatives, including indolizidine alkaloids. Finally, we show that NHP is glycosylated in Arabidopsis to form a hexose-conjugate, and then discuss open questions in Pip/NHP-related research.

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“…Previous studies have demonstrated that S. graminum feeding induced SA-and JA-dependent defence pathways in sorghum (Sorghum bicolor) [28], and reactive oxygen species (ROS) levels, peroxidase (POD) and laccase activities were also increased in switchgrass (Panicum virgatum) after S. graminum feeding [29]. However, few studies have been conducted to identify the defence mechanisms in wheat in response to S. graminum feeding, and the mechanisms underlying the induction of damage by S. graminum infestation are still unclear.…”

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confidence: 99%

Transcriptome analysis reveals rapid defence responses in wheat induced by phytotoxic aphid Schizaphis graminum feeding

Zhang

Wang

et al. 2020

Preprint

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Background Schizaphis graminum is one of the most important and devastating cereal aphids worldwide, and its feeding can cause chlorosis and necrosis in wheat. However, little information is available on the wheat defence responses triggered by S. graminum feeding at the molecular level. Results Here, we collected and analysed transcriptome sequencing data from leaf tissues of wheat infested with S. graminum at 2, 6, 12, 24 and 48 hpi (hours post infestation). A total of 44,835 genes were either up- or downregulated and differed significantly in response to aphid feeding. The expression levels of a number of genes (9,761 genes) were significantly altered within 2 hpi and continued to change during the entire 48 h experiment. Gene Ontology analysis showed that the downregulated DEGs were mainly enriched in photosynthesis and light harvesting, and the total chlorophyll content in wheat leaves was also significantly reduced after S. graminum infestation at 24 and 48 hpi. However, a number of related genes of the salicylic acid (SA)-mediated defence signalling pathway and MAPK-WRKY pathway were significantly upregulated at early feeding time points (2 and 6 hpi). In addition, the gene expression and activity of antioxidant enzymes, such as peroxidase and superoxide dismutase, were rapidly increased at 2, 6 and 12 hpi. DAB staining results showed that S. graminum feeding induced hydrogen peroxide (H 2 O 2 ) accumulation at the feeding sites at 2 hpi, and increased H 2 O 2 production was detected with the increases in aphid feeding time. Pretreatment with diphenylene iodonium, an NADPH oxidase inhibitor, repressed the H 2 O 2 accumulation and expression levels of SA-associated defence genes in wheat. Conclusions Our transcriptomic analysis revealed that defence-related pathways and oxidative stress in wheat were rapidly induced within hours after the initiation of aphid feeding. Additionally, NADPH oxidase plays an important role in aphid-induced defence responses and H 2 O 2 accumulation in wheat. These results provide valuable insight into the dynamic transcriptomic responses of wheat leaves to phytotoxic aphid feeding and the molecular mechanisms of aphid-plant interactions.

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Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs

Cited by 34 publications

References 123 publications

Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum

Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum

l‐lysine metabolism to N‐hydroxypipecolic acid: an integral immune‐activating pathway in plants

Transcriptome analysis reveals rapid defence responses in wheat induced by phytotoxic aphid Schizaphis graminum feeding

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