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Seed priming is a state-of-the-art, low-cost, and environment-friendly strategy to improve seed germination, seed vigor, abiotic and biotic stress tolerance, and the yield of field and horticultural crops. Seed priming involves imbibing the seeds in a priming solution under a desired set of environmental conditions for a period followed by drying before the radicle protrusion. Several seed priming approaches including hydropriming, osmopriming, bio-priming, hormonal priming, nutrient priming, nanoparticle priming, and electropriming can be effectively employed under different environmental conditions to improve crop growth and stress resilience. Seed priming is known to trigger enzymatic, hormonal, physiological, transcriptomic, metabolomic, and proteomic regulations in seed embryos during seed germination and plant growth, which leads to faster and synchronized seed germination and higher abiotic and biotic stress tolerance in crop plants. Furthermore, seed priming can induce cross-tolerance between abiotic and biotic stressors and induce stress memory for higher resilience of the next generation to environmental stresses. The present review paper discusses the applications of seed priming in biotic and abiotic stress tolerance and the underlying abiotic and biotic stress tolerance physiological, biochemical, and molecular mechanisms of seed priming. Furthermore, we discuss the current challenges/bottlenecks in the widespread application of seed priming in crop production.

Key messageInteractions among phytohormones are essential for providing tolerance of sorghum plants to aphids.Plant’s encounter with insect herbivores trigger defense signaling networks that fine-tune plant resistance to insect pests. Although it is well established that phytohormones contribute to antixenotic- and antibiotic-mediated resistance to insect pests, their role in conditioning plant tolerance, the most durable and promising category of host plant resistance, is largely unknown. Here, we screened a panel of sorghum (Sorghum bicolor) inbred lines to identify and characterize sorghum tolerance to sugarcane aphids (SCA; Melanaphis sacchari Zehntner), a relatively new and devastating pest of sorghum in the United States. Our results suggest that the sorghum genotype SC35, the aphid-tolerant line identified among the sorghum genotypes, displayed minimal plant biomass loss and a robust photosynthetic machinery, despite supporting higher aphid population. Phytohormone analysis revealed significantly higher basal levels of 12-oxo-phytodienoic acid, a precursor in the jasmonic acid biosynthesis pathway, in the sorghum SCA-tolerant SC35 plants. Salicylic acid accumulation appeared as a generalized plant response to aphids in sorghum plants, however, SCA feeding-induced salicylic acid levels were unaltered in the sorghum tolerant genotype. Conversely, basal levels of abscisic acid and aphid feeding-induced cytokinins were accumulated in the SCA-tolerant sorghum genotype. Our findings imply that the aphid-tolerant sorghum genotype tightly controls the relationship among phytohormones, as well as provide significant insights into the underlying mechanisms that contribute to plant tolerance to sap-sucking aphids.

Background The 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. Results 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. Conclusions 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.

The corn leaf aphid (CLA; Rhopalosiphum maidis) is a phloem sap-sucking insect that attacks many cereal crops, including maize (Zea mays). We previously showed that the maize inbred line Mp708, which was developed by classical plant breeding, provides enhanced resistance to CLA. Here, using electrophysiological monitoring of aphid feeding behavior, we demonstrate that Mp708 provides phloem-mediated resistance to CLA. Furthermore, feeding by CLA on Mp708 plants enhanced callose deposition, a potential defense mechanism utilized by plants to limit aphid feeding and subsequent colonization. In maize, benzoxazinoids (BX) or BX-derived metabolites contribute to enhanced callose deposition by providing heightened resistance to CLA. However, BX and BX-derived metabolites were not significantly altered in CLA-infested Mp708 plants, indicating BX-independent defense against CLA. Evidence presented here suggests that the constitutively higher levels of 12-oxo-phytodienoic acid (OPDA) in Mp708 plants contributed to enhanced callose accumulation and heightened CLA resistance. OPDA enhanced the expression of ethylene biosynthesis and receptor genes, and the synergistic interactions of OPDA and CLA feeding significantly induced the expression of the transcripts encoding Maize insect resistance1-Cysteine Protease, a key defensive protein against insect pests, in Mp708 plants. Furthermore, exogenous application of OPDA on maize jasmonic acid-deficient plants caused enhanced callose accumulation and heightened resistance to CLA, suggesting that the OPDA-mediated resistance to CLA is independent of the jasmonic acid pathway. We further demonstrate that the signaling function of OPDA, rather than a direct toxic effect, contributes to enhanced CLA resistance in Mp708.

Plants undergo dynamic metabolic changes at the cellular level upon insect infestation to better defend themselves. Phenylpropanoids, a hub of secondary plant metabolites, encompass a wide range of compounds that can contribute to insect resistance. Here, the role of sorghum ( Sorghum bicolor ) phenylpropanoids in providing defense against the chewing herbivore, fall armyworm (FAW), Spodoptera frugiperda , was explored. We screened a panel of nested association mapping (NAM) founder lines against FAW and identified SC1345 and Ajabsido as most resistant and susceptible lines to FAW, respectively, compared to reference parent, RTx430. Gene expression and metabolomic studies suggested that FAW feeding suppressed the expression level of genes involved in monolignol biosynthetic pathway and their associated phenolic intermediates at 10 days post infestation. Further, SC1345 genotype displayed elevated levels of flavonoid compounds after FAW feeding for 10 days, suggesting a diversion of precursors from lignin biosynthesis to the flavonoid pathway. Additionally, bioassays with sorghum lines having altered levels of flavonoids provided genetic evidence that flavonoids are crucial in providing resistance against FAW. Finally, the application of FAW regurgitant elevated the expression of genes associated with the flavonoid pathway in the FAW-resistant SC1345 genotype. Overall, our study indicates that a dynamic regulation of the phenylpropanoid pathway in sorghum plants imparts resistance against FAW.

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

The greenbug, Schizaphis graminum , is a serious pest of sorghum ( Sorghum bicolor ). For the past several decades, resistant sorghum hybrids have been used to control greenbug populations. However, the durability of plant resistance is frequently challenged by evolution of new greenbug biotypes, and there is a continuous need for screening of resistant germplasm for its effective management in the field. Natural variation in sorghum plants/populations provides distinct approaches to identify novel sources of resistance against greenbugs. In this study, we used the recently developed sorghum nested association mapping (NAM) population parental lines to understand sources of sorghum resistance to greenbugs. Using choice and no-choice assays, we have identified SC265 and Segaolane as the resistant and susceptible lines, respectively, to greenbugs compared to the wild-type plants. The Electrical Penetration Graph (EPG) analysis revealed that the greenbugs spent significantly lesser time in the xylem and sieve element phases while feeding on the resistant NAM parental line, SC265, compared to the susceptible (Segaolane) and wild-type (RTx430) sorghum lines. In addition, the EPG results indicated that there is no significant difference in the time to first probe, time to reach first sieve element, pathway phase, and non-probing phase among the three sorghum plants, which suggests that the resistance factors present in the vascular tissues of the resistant line (SC265) potentially contribute to the resistance mechanisms against greenbugs. Overall, SC265 NAM parental line showed a combination of antixenotic and antibiotic-mediated resistance mechanisms against greenbugs, whereas the susceptible line Segaolane displayed the least resistance to greenbugs.

Main conclusionQuantification of cuticular waxes coupled with insect bioassays and feeding behavior analysis demonstrate that long-chain C32 fatty alcohol impacts host plant selection by aphids.Cuticular waxes constitute the first point of contact between plants and their environment, and it also protect plants from external stresses. However, the role of waxes in Sorghum bicolor (sorghum) against sugarcane aphid (Melanaphis sacchari), a relatively new and devastating pest of sorghum in the U.S., is not fully understood. In this study, we monitored sugarcane aphid behavior on two genotypes of young sorghum plants with different wax chemistry: a wild-type plant (bloom) with lower C32 alcohol cuticular wax, and a mutant plant (bloomless) with 1.6 times the amount of wax compared to wild-type plants. No-choice aphid bioassays revealed that sugarcane aphid reproduction did not vary between wild-type and the bloomless plants. Electrical Penetration Graph (EPG) monitoring indicated that the sugarcane aphids spent comparable amount of time feeding from the sieve elements of the wild-type and bloomless plants. However, aphids spent more time feeding on the xylem sap of the bloomless plants compared to the wild-type plants. Furthermore, aphid choice assays revealed that the sugarcane aphids preferred to settle on bloomless compared to wild-type plants. Overall, our results suggest that cuticular waxes on young sorghum leaves play a critical role in influencing host plant selection by sugarcane aphids.

Main conclusionInsect herbivores of different feeding guilds induced sorghum defenses through differential mechanisms, regardless of the order of herbivore arrival on sorghum plants.Sorghum, one of the world’s most important cereal crops, suffers severe yield losses due to attack by insects of different feeding guilds. In most instances, the emergence of these pests are not secluded incidents and are followed by another or can also co-infest host plants. Sugarcane aphid (SCA) and fall armyworm (FAW) are the two most important destructive pests of sorghum, which belongs to sap-sucking and chewing feeding guilds, respectively. While the order of the herbivore arriving on the plants has been found to alter the defense response to subsequent herbivores, this is seldom studied with herbivores from different feeding guilds. In this study, we investigated the effects of sequential herbivory of FAW and SCA on sorghum defense responses and their underlying mechanism(s). Sequential feeding on the sorghum RTx430 genotype by either FAW primed–SCA or SCA primed–FAW were monitored to unravel the mechanisms underlying defense priming, and its mode of action. Regardless of the order of herbivore arrival on sorghum RTx430 plants, significant defense induction was observed in the primed state compared to the non-primed condition, irrespective of their feeding guild. Additionally, gene expression and secondary metabolite analysis revealed differential modulation of the phenylpropanoid pathway upon insect attack by different feeding guilds. Our findings suggest that priming in sorghum plants upon sequential herbivory induces defense by the accumulation of the total flavonoids and lignin/salicylic acid in FAW primed–SCA and SCA primed–FAW interaction, respectively.

Sorghum (Sorghum bicolor) is one of the most important monocot crops cultivated worldwide and known for its versatility as a food, forage, and bioenergy crop. Sugarcane aphid (SCA; Melanaphis sacchari Zehntner) is considered a major threat to sorghum production, which severely damages the plant by sucking sap from leaves, thereby reducing its photosynthetic ability. Although several studies have been focused on identification of sorghum resistant/tolerant varieties to SCA, very little is known about how sorghum mounts direct defenses against SCA. In the current study, we screened a panel of sorghum nested association mapping (NAM) founder lines to identify and characterize sorghum resistance/tolerance mechanisms to SCA. We identified sorghum genotype SC35 as the aphid-tolerant line among the different sorghum genotypes that displayed minimal plant biomass loss and a robust photosynthetic machinery, despite supporting higher aphid population. Phytohormone analysis revealed significantly higher basal levels of 12-oxo-phytodienoic acid, a precursor in the jasmonic acid biosynthesis pathway, and increased levels of cytokinins in the sorghum SCA-tolerant SC35 plants. Next, we found SC265 genotype demonstrates a combination of antibiosis- and antixenosis-mediated resistance mechanisms to SCA. Feeding behavior studies using electrical penetration graph (EPG) technique revealed that SCA spent less time in the sieve element phase and more time in the pathway phase of SC265, compared to reference line, RTx430 and susceptible line, SC1345. Furthermore, phytohormonal analysis suggests that the higher constitutive and SCA feeding-induced levels of salicylic acid in SC265 can provide defenses against aphids. Proteome profiling of SC265 after SCA infestation at days 1 and 7 revealed the suppression of plant defense-related proteins and upregulation of plant defense and signaling-related proteins, respectively. In addition, we utilized the sorghum brown midrib (bmr) mutants impaired in lignin biosynthesis to understand the defense mechanisms against SCA. We found that bmr12 impaired in caffeic acid O‐methyltransferase (COMT) activity, involved in the synthesis of S-lignin subunits, provides resistance to SCA. Results from this work will help us to better understand the sorghum defense signaling mechanisms against phloem-feeding insects.