Plants are attacked by multiple insect pest species and insect herbivory can alter plant defense mechanisms. The plant defense responses to a specific herbivore may also contribute to the herbivore growth/survival on plants. Feeding by one insect species can modulate the plant defenses, which can either facilitate or hamper the colonization of subsequent incoming insects. However, little is known about the effect of sequential herbivory on sorghum plants. In this study, we demonstrate that a specialist aphid, sugarcane aphid (SCA; Melanaphis sacchari ) grows faster on sorghum than a generalist aphid species, greenbug (GB; Schizaphis graminum ). We also determined how the pre-infestation of SCA on sorghum affected the invasion of GB and vice-versa . Our sequential herbivory experiments revealed that SCA reproduction was lower on GB-primed sorghum plants, however, the reverse was not true. To assess the differences in plant defenses induced by specialist vs. generalist aphids, we monitored the expression of salicylic acid (SA) and jasmonic acid (JA) marker genes, and flavonoid biosynthetic pathway genes after 48 h of aphid infestation. The results indicated that GB infestation induced higher expression of SA and JA-related genes, and flavonoid pathway genes ( DFR , FNR , and FNSII ) compared to SCA infestation. Overall, our results suggested that GB-infested plants activate the plant defenses via phytohormones and flavonoids at early time points and hampers the colonization of incoming SCA, as well as explain the reproductive success of SCA compared to GB.
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Temporal transcriptomic profiling elucidates sorghum defense mechanisms against sugarcane aphids
The sugarcane aphid (SCA;
We used RNA-sequencing approach to identify the global transcriptomic responses to aphid infestation on RTx430, SC265, and SC1345 plants at early time points 6, 24, and 48 h post infestation (hpi) and after extended period of SCA feeding for 7 days. Aphid feeding on the SCA-resistant line upregulated the expression of 3827 and 2076 genes at early and late time points, respectively, which was relatively higher compared to RTx430 and SC1345 plants. Co-expression network analysis revealed that aphid infestation modulates sorghum defenses by regulating genes corresponding to phenylpropanoid metabolic pathways, secondary metabolic process, oxidoreductase activity, phytohormones, sugar metabolism and cell wall-related genes. There were 187 genes that were highly expressed during the early time of aphid infestation in the SCA-resistant line, including genes encoding leucine-rich repeat (LRR) proteins, ethylene response factors, cell wall-related, pathogenesis-related proteins, and disease resistance-responsive dirigent-like proteins. At 7 days post infestation (dpi), 173 genes had elevated expression levels in the SCA-resistant line and were involved in sucrose metabolism, callose formation, phospholipid metabolism, and proteinase inhibitors.
In summary, our results indicate that the SCA-resistant line is better adapted to activate early defense signaling mechanisms in response to SCA infestation because of the rapid activation of the defense mechanisms by regulating genes involved in monolignol biosynthesis pathway, oxidoreductase activity, biosynthesis of phytohormones, and cell wall composition. This study offers further insights to better understand sorghum defenses against aphid herbivory.
- Award ID(s):
- 1845588
- NSF-PAR ID:
- 10438893
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- BMC Genomics
- Volume:
- 24
- Issue:
- 1
- ISSN:
- 1471-2164
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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P. palmivora- resistant genotype SCA 6 (Additional file 1: Tables S1-S5), deposited in GenBank under accessions CP139290-CP139299. We then used this high-quality assembly to combine RNA and whole-genome sequencing data to discover several genes and pathways associated with resistance. Many of these are unique, i.e., differentially regulated in only one of the four populations (diverged 40 k–900 k generations). Among the pathways shared across all populations is phenylpropanoid biosynthesis, a metabolic pathway with well-documented roles in plant defense. One gene in this pathway, caffeoyl shikimate esterase (CSE), was upregulated across all four populations following pathogen treatment, indicating its broad importance for cacao’s defense response. Further experimental evidence suggests this gene hydrolyzes caffeoyl shikimate to create caffeic acid, an antimicrobial compound and known inhibitor ofPhytophthora spp .Conclusions Our results indicate most expression variation associated with resistance is unique to populations. Moreover, our findings demonstrate the value of using a broad sample of evolutionarily diverged populations for revealing the genetic bases of cacao resistance to
P. palmivora . This approach has promise for further revealing and harnessing valuable genetic resources in this and other long-generation plants. -
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