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Summary Lignin, a complex heterogenous polymer present in virtually all plant cell walls, plays a critical role in protecting plants from various stresses. However, little is known about how lignin modifications in sorghum will impact plant defense against sugarcane aphids (SCA), a key pest of sorghum.We utilized the sorghumbrown midrib(bmr) mutants, which are impaired in monolignol synthesis, to understand sorghum defense mechanisms against SCA. We found that loss ofBmr12function and overexpression (OE) ofBmr12provided enhanced resistance and susceptibility to SCA, respectively, as compared with wild‐type (WT; RTx430) plants.Monitoring of the aphid feeding behavior indicated that SCA spent more time in reaching the first sieve element phase onbmr12plants compared with RTx430 andBmr12‐OE plants. A combination of transcriptomic and metabolomic analyses revealed thatbmr12plants displayed altered auxin metabolism upon SCA infestation and specifically, elevated levels of auxin conjugate indole‐3‐acetic acid–aspartic acid (IAA–Asp) were observed inbmr12plants compared with RTx430 andBmr12‐OE plants. Furthermore, exogenous application of IAA–Asp restored resistance inBmr12‐OE plants, and artificial diet aphid feeding trial bioassays revealed that IAA–Asp is associated with enhanced resistance to SCA.Our findings highlight the molecular underpinnings that contribute to sorghumbmr12‐mediated resistance to SCA. 

Gut microbiomes profoundly influence insect health and mediate interactions between plant hosts and their environments. Insects, including aphids, harbour diverse obligate symbionts that synthesize essential nutrients and facultative symbionts that enhance host fitness in specific ecological contexts. Sorghum (Sorghum bicolor) is a significant cereal crop cultivated worldwide that has been negatively affected by the presence of an invasive piercing-sucking insect pest, the sugarcane aphid (SCA; Melanaphis sacchari). We previously identified SC265 and SC1345 as the resistant and susceptible sorghum lines, respectively, among the founder nested association mapping (NAM) population. Here, using these resistant and susceptible lines, we explored variations in the SCA gut microbiome when they feed on two different sorghum lines with varied resistance levels. Analyses after excluding the obligate endosymbiont Buchnera aphidicola from the dataset showed a significant difference in microbial diversity and composition between resistant and susceptible sorghum lines 7- and 14 days post aphid infestation. Our results indicate that the SCA fed on susceptible and resistant sorghum lines had Pseudomonadaceae and Rhizobiaceae, respectively, as the most abundant bacterial families. Differences in gut microbial community composition were underscored by alpha diversity metrics and beta diversity compositional analyses. These findings contribute to our understanding of the intricate interplay between plant and aphid microbiomes, shedding light on potential avenues to bolster sorghum resistance to SCA. 

ABSTRACT Sorghum (Sorghum bicolor) plays a critical role in global agriculture, serving as a staple food source and contributing significantly to various industries. However, sorghum cultivation faces significant challenges, particularly from pests like the sugarcane aphid (SCA), which can cause substantial damage to crops. In this study, we investigated the role of the caffeoyl coenzyme‐AO‐methyltransferase (CCoAOMT) gene in sorghum defense against SCA. Feeding by SCA induced the expression of theSbCCoAOMTgene, which is involved in the monolignol biosynthesis pathway. Aphid no‐choice and choice bioassays revealed thatSbCCoAOMToverexpression in sorghum resulted in reduced SCA reproduction and decreased aphid settling, respectively, compared to wild‐type (RTx430) plants. Furthermore, electrical penetration graph (EPG) studies revealed thatSbCCoAOMToverexpression restricts aphid feeding from the sieve elements. SCA feeding also induced the accumulation of lignin in sorghum wild‐type andSbCCoAOMToverexpression plants. Moreover, artificial diet aphid feeding bioassays with hydroxycinnamic acids, ferulic and sinapic acids, showed direct adverse effects on SCA reproduction. Our findings highlight the potential of genetic modification to enhance sorghum resistance to SCA and emphasize the importance of lignin‐related genes in plant defense mechanisms. This study offers valuable insights into developing aphid‐resistant sorghum varieties and suggests avenues for further research on enhancing plant defenses against biotic stresses. 

Abstract During the last decade, the sorghum aphid (Melanaphis sorghi), previously identified as sugarcane aphid (Melanaphis sacchari), became a serious pest of sorghum, spreading to all sorghum‐producing regions in the United States, Mexico, and South America, where crop losses of 50%–100% have been reported. Developing sorghum cultivars with resistance to this insect is the most sustainable strategy for long‐term pest management. To design cultivars with aphid resistance, comprehensively understanding the mechanisms underlying aphid survival, host plant resistance, and aphid–sorghum interactions is critical. In this review, we summarize the comprehensive efforts to characterize the aphid populations as well as their interaction with sorghum plants via hormonal pathways that trigger various genes including leucine rich repeats, WRKY transcription factors, lipoxygenases, calmodulins, and others. We discuss efforts made during the last decade to identify specific genomic regions and candidate genes that confer aphid resistance, as well as describe recent successes and potential challenges in breeding for aphid resistance. Furthermore, we discuss the use of disruptive technologies like high‐throughput phenotyping, artificial intelligence, or machine learning for developing aphid resistant sorghum cultivars. Integration of these new technologies has the potential to accelerate the development and design of novel traits that confer durable aphid resistance in new sorghum cultivars to defend sorghum against new aphid genotype development. 

Abstract BackgroundThe sugarcane aphid (SCA;Melanaphis sacchari) has emerged as a key pest on sorghum in the United States that feeds from the phloem tissue, drains nutrients, and inflicts physical damage to plants. Previously, it has been shown that SCA reproduction was low and high on sorghum SC265 and SC1345 plants, respectively, compared to RTx430, an elite sorghum male parental line (reference line). In this study, we focused on identifying the defense-related genes that confer resistance to SCA at early and late time points in sorghum plants with varied levels of SCA resistance. ResultsWe 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. ConclusionsIn 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.