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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. 

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 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. 

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. 

The precursors and derivatives of jasmonic acid (JA) contribute to plant protective immunity to insect attack. However, the role of JA in sorghum (Sorghum bicolor) defense against sugarcane aphid (SCA; Melanaphis sacchari), which is considered a major threat to sorghum production, remains elusive. Sorghum SC265, previously identified as a SCA resistant genotype among the sorghum nested association mapping founder lines, transiently increased JA at early stages of aphid feeding and deterred aphid settling. Monitoring of aphid feeding behavior using electropenetrography, a technique to unveil feeding process of piercing-sucking insects, revealed that SC265 plants restricted SCA feeding from the phloem sap. However, exogenous application of JA attenuated the resistant phenotype and promoted improved aphid feeding and colonization on SC265 plants. This was further confirmed with sorghum JA-deficient plants, in which JA deficiency promoted aphid settling, however, it also reduced aphid feeding from the phloem sap and curtailed SCA population. Exogenous application of JA caused enhanced feeding and aphid proliferation on JA-deficient plants, suggesting that JA promotes aphid growth and development. SCA feeding on JA-deficient plants altered the sugar metabolism and induced the levels of fructose and trehalose compared to wild-type plants. Furthermore, aphid artificial diet containing fructose and trehalose curtailed aphid growth and reproduction. Our findings underscore a previously unknown dichotomous role of JA, which may have opposing effects by deterring aphid settling during early stage and enhancing aphid’s proliferative capacity during later-stages of aphid colonization on sorghum plants.