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      Global Responses of Resistant and Susceptible Sorghum ( Sorghum bicolor) to Sugarcane Aphid ( Melanaphis sacchari)

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          Abstract

          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 F 1 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 F 1 plants. Aphid resistance from RTx2783 segregated as a single dominant locus in the F 2 generation, which will enable breeders to rapidly develop sugarcane aphid-resistant hybrids using RTx2783 as the male parent.

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          Plant responses to insect herbivory: the emerging molecular analysis.

          Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the diversity of responses elicited by herbivore attack.
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            Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid.

            When attacked by a phloem-feeding greenbug aphid (Schizaphis graminum), sorghum (Sorghum bicolor) activates jasmonic acid (JA)- and salicylic acid (SA)-regulated genes, as well as genes outside known wounding and SA signaling pathways. A collection of 672 cDNAs was obtained by differential subtraction with cDNAs prepared from sorghum seedlings infested by greenbug aphids and those from uninfested seedlings. Subsequent expression profiling using DNA microarray and northern-blot analyses identified 82 transcript types from this collection responsive to greenbug feeding, methyl jasmonate (MeJA), or SA application. DNA sequencing analyses indicated that these encoded proteins functioning in direct defense, defense signaling, oxidative burst, secondary metabolism, abiotic stress, cell maintenance, and photosynthesis, as well as proteins of unknown function. In response to insect feeding, sorghum increased transcript abundance of numerous defense genes, with some SA-dependent pathogenesis-related genes responding to greenbug more strongly than to SA. In contrast, only weak induction of MeJA-regulated defense genes was observed after greenbug treatment. However, infestation tests confirmed that JA-regulated pathways were effective in plant defense against greenbugs. Activation of certain transcripts exclusively by greenbug infestation was observed, and may represent unique signal transduction events independent of JA- and SA-regulated pathways. Results indicate that plants coordinately regulate defense gene expression when attacked by phloem-feeding aphids, but also suggest that aphids are able to avoid triggering activation of some otherwise potentially effective plant defensive machinery, possibly through their particular mode of feeding.
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              Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways.

              Under herbivore attack plants mount a defence response characterized by the accumulation of secondary metabolites and inhibitory proteins. Significant changes are observed in the transcriptional profiles of genes encoding enzymes of primary metabolism. Such changes have often been interpreted in terms of a requirement for an increased investment of resources to 'fuel' the synthesis of secondary metabolites. While enhanced secondary metabolism undoubtedly exerts an influence on primary metabolism, accumulating evidence suggests that rather than stimulating photosynthesis insect herbivory reduces photosynthetic carbon fixation and this response occurs by a re-programming of gene expression. Within this context, reactive oxygen species (ROS) and reductant/oxidant (redox) signalling play a central role. Accumulating evidence suggests that ROS signalling pathways are closely interwoven with hormone-signalling pathways in plant-insect interactions. Here we consider how insect infestation impacts on the stress signalling network through effects on ROS and cellular redox metabolism with particular emphasis on the roles of ROS in the plant responses to phloem-feeding insects. © 2011 Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                22 February 2019
                2019
                : 10
                : 145
                Affiliations
                [1] 1Wheat, Sorghum and Forage Research Unit, USDA-ARS , Lincoln, NE, United States
                [2] 2Department of Agronomy and Horticulture, University of Nebraska–Lincoln , Lincoln, NE, United States
                [3] 3Department of Entomology, University of Nebraska–Lincoln , Lincoln, NE, United States
                Author notes

                Edited by: Brigitte Mauch-Mani, University of Neuchâtel, Switzerland

                Reviewed by: Rosa Rao, University of Naples Federico II, Italy; Anna-Maria Botha-Oberholster, Stellenbosch University, South Africa

                *Correspondence: Scott E. Sattler, scott.sattler@ 123456ars.usda.gov

                Present address: Erin D. Scully, Stored Product Insect and Engineering Research Unit, Center for Grain and Animal Health Research, USDA-ARS, Manhattan, KS, United States

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.00145
                6396740
                30853964
                524adb9f-f70f-484e-b2de-82ede3ab431e
                Copyright © 2019 Tetreault, Grover, Scully, Gries, Palmer, Sarath, Louis and Sattler.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 September 2018
                : 28 January 2019
                Page count
                Figures: 11, Tables: 2, Equations: 0, References: 80, Pages: 19, Words: 0
                Funding
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                sugarcane aphid,sorghum,plant–insect interactions,melanaphis sacchari,sorghum bicolor

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