Plants produce diverse specialized metabolites (SMs), but the genes responsible for their production and regulation remain largely unknown, hindering efforts to tap plant pharmacopeia. Given that ...genes comprising SM pathways exhibit environmentally dependent coregulation, we hypothesized that genes within a SM pathway would form tight associations (modules) with each other in coexpression networks, facilitating their identification. To evaluate this hypothesis, we used 10 global coexpression data sets, each a meta-analysis of hundreds to thousands of experiments, across eight plant species to identify hundreds of coexpressed gene modules per data set. In support of our hypothesis, 15.3 to 52.6% of modules contained two or more known SM biosynthetic genes, and module genes were enriched in SM functions. Moreover, modules recovered many experimentally validated SM pathways, including all six known to form biosynthetic gene clusters (BGCs). In contrast, bioinformatically predicted BGCs (i.e., those lacking an associated metabolite) were no more coexpressed than the null distribution for neighboring genes. These results suggest that most predicted plant BGCs are not genuine SM pathways and argue that BGCs are not a hallmark of plant specialized metabolism. We submit that global gene coexpression is a rich, largely untapped resource for discovering the genetic basis and architecture of plant natural products.
Plants are constantly exposed to microorganisms in the environment and, as a result, have evolved intricate mechanisms to recognize and defend themselves against potential pathogens. One of these ...responses is the downregulation of photosynthesis and other processes associated with primary metabolism that are essential for plant growth. It has been suggested that the energy saved by downregulation of primary metabolism is diverted and used for defense responses. However, several studies have shown that upregulation of primary metabolism also occurs during plant-pathogen interactions. We propose that upregulation of primary metabolism modulates signal transduction cascades that lead to plant defense responses. In support of this thought, we here compile evidence from the literature to show that upon exposure to pathogens or elicitors, plants induce several genes associated with primary metabolic pathways, such as those involved in the synthesis or degradation of carbohydrates, amino acids and lipids. In addition, genetic studies have confirmed the involvement of these metabolic pathways in plant defense responses. This review provides a new perspective highlighting the relevance of primary metabolism in regulating plant defense against pathogens with the hope to stimulate further research in this area.
The bird cherry-oat aphid (
Rhopalosiphum padi
) is one of the most destructive insect pests in wheat production. To reduce aphid damage, wheat plants have evolved various chemical and physical ...defense mechanisms. Although these mechanisms have been frequently reported, much less is known about their effectiveness. The tetraploid wild emmer wheat (WEW;
Triticum turgidum
ssp.
dicoccoides
), one of the progenitors of domesticated wheat, possesses untapped resources from its numerous desirable traits, including insect resistance. The goal of this research was to determine the effectiveness of trichomes (physical defense) and benzoxazinoids (BXDs; chemical defense) in aphid resistance by exploiting the natural diversity of WEW. We integrated a large dataset composed of trichome density and BXD abundance across wheat genotypes, different leaf positions, conditions (constitutive and aphid-induced), and tissues (whole leaf and phloem sap). First, we evaluated aphid reproduction on 203 wheat accessions and found large variation in this trait. Then, we chose eight WEW genotypes and one domesticated durum wheat cultivar for detailed quantification of the defense mechanisms across three leaves. We discovered that these defense mechanisms are influenced by both leaf position and genotype, where aphid reproduction was the highest on leaf-1 (the oldest), and trichome density was the lowest. We compared the changes in trichome density and BXD levels upon aphid infestation and found only minor changes relative to untreated plants. This suggests that the defense mechanisms in the whole leaf are primarily anticipatory and unlikely to contribute to aphid-induced defense. Next, we quantified BXD levels in the phloem sap and detected a significant induction of two compounds upon aphid infestation. Moreover, evaluating aphid feeding patterns showed that aphids prefer to feed on the oldest leaf. These findings revealed the dynamic response at the whole leaf and phloem levels that altered aphid feeding and reproduction. Overall, they suggested that trichomes and the BXD 2,4-dihydroxy-7- methoxy-1,4-benzoxazin-3-one (DIMBOA) levels are the main factors determining aphid resistance, while trichomes are more effective than BXDs. Accessions from the WEW germplasm, rich with trichomes and BXDs, can be used as new genetic sources to improve the resistance of elite wheat cultivars.
Young wheat plants are continuously exposed to herbivorous insect attack. To reduce insect damage and maintain their growth, plants evolved different defense mechanisms, including the biosynthesis of ...deterrent compounds named benzoxazinoids, and/or trichome formation that provides physical barriers. It is unclear whether both of these mechanisms are equally critical in providing an efficient defense for wheat seedlings against aphids-an economically costly pest in cereal production.
In this study, we compared the transcriptome, metabolome, benzoxazinoids, and trichome density of three selected wheat genotypes, with a focus on differences related to defense mechanisms. We chose diverse wheat genotypes: two tetraploid wheat genotypes, domesticated durum 'Svevo' and wild emmer 'Zavitan,' and one hexaploid bread wheat, 'Chinese Spring.' The full transcriptomic analysis revealed a major difference between the three genotypes, while the clustering of significantly different genes suggested a higher similarity between the two domesticated wheats than between either and the wild wheat. A pathway enrichment analysis indicated that the genes associated with primary metabolism, as well as the pathways associated with defense such as phytohormones and specialized metabolites, were different between the three genotypes. Measurement of benzoxazinoid levels at the three time points (11, 15, and 18 days after germination) revealed high levels in the two domesticated genotypes, while in wild emmer wheat, they were below detection level. In contrast to the benzoxazinoid levels, the trichome density was dramatically higher in the wild emmer than in the domesticated wheat. Lastly, we tested the bird cherry-oat aphid's (Rhopalosiphum padi) performance and found that Chinese Spring is more resistant than the tetraploid genotypes.
Our results show that benzoxazinoids play a more significant defensive role than trichomes. Differences between the abundance of defense mechanisms in the wild and domesticated plants were observed in which wild emmer possesses high physical defenses while the domesticated wheat genotypes have high chemical defenses. These findings provide new insights into the defense adaptations of wheat plants against aphids.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The expression pattern of any pair of genes may be negatively correlated, positively correlated, or not correlated at all in response to different stresses and even different progression stages of ...the stress. This makes it difficult to identify such relationships by classical statistical tools such as the Pearson correlation coefficient. Hence, dedicated bioinformatics approaches that are able to identify groups of cues in which there is a positive or negative expression correlation between pairs or groups of genes are called for. We herein introduce and discuss a bioinformatics approach, termed Gene Coordination, that is devoted to the identification of specific or multiple cues in which there is a positive or negative coordination between pairs of genes and can further incorporate additional coordinated genes to form large coordinated gene networks. We demonstrate the utility of this approach by providing a case study in which we were able to discover distinct expression behavior of the energy-associated gene network in response to distinct biotic and abiotic stresses. This bioinformatics approach is suitable to a broad range of studies that compare treatments versus controls, such as effects of various cues, or expression changes between a mutant and the control wild-type genotype.
Aphids are major pests in cereal crops that cause direct and indirect damage leading to yield reduction. Despite the fact that wheat provides 20% of the world's caloric and protein diet, its ...metabolic responses to aphid attack, in general, and specifically its production of benzoxazinoid defense compounds are poorly understood. The objective of this study was to compare the metabolic diversity of durum wheat seedlings (Triticum turgidum ssp. durum) under attack by three different cereal aphids: i) the English grain aphid (Sitobion avenae Fabricius), ii) the bird cherry-oat aphid (Rhopalosiphum padi L.), and iii) the greenbug aphid (Schizaphis graminum Rondani), which are some of the most destructive aphid species to wheat. Insect progeny bioassays and metabolic analyses using chromatography/Q-Exactive/mass spectrometry non-targeted metabolomics and a targeted benzoxazinoid profile were performed on infested leaves. The insect bioassays revealed that the plants were susceptible to S. graminum, resistant to S. avenae, and mildly resistant to R. padi. The metabolic analyses of benzoxazinoids suggested that the predominant metabolites DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin- 3-one) and its glycosylated form DIMBOA-glucoside (Glc) were significantly induced upon both S. avenae, and R. padi aphid feeding. However, the levels of the benzoxazinoid metabolite HDMBOA-Glc (2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside) were enhanced due to the feeding of S. avenae and S. graminum aphids, to which Svevo was the most resistant and the most susceptible, respectively. The results showed a partial correlation between the induction of benzoxazinoids and aphid reproduction. Overall, our observations revealed diverse metabolic responses of wheat seedlings to cereal aphid feeding.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Key message
A combined transcriptomic and metabolic analysis of
Setaria viridis
leaves responding to aphid infestation was used to identify genes related to serotonin biosynthesis.
Setaria viridis
...(green foxtail), a short life-cycle C4 plant in the Poaceae family, is the wild ancestor of
Setaria italica
(foxtail millet), a resilient crop that provides good yields in dry and marginal land. Although
S. viridis
has been studied extensively in the last decade, the molecular mechanisms of insect resistance in this species remain under-investigated. To address this issue, we performed a metabolic analysis of
S. viridis
and discovered that these plants accumulate the tryptophan-derived compounds tryptamine and serotonin. To elucidate the defensive functions of serotonin,
Rhophalosiphum padi
(bird cherry-oat aphids) were exposed to this compound, either by exogenous application to the plant medium or with artificial diet bioassays. In both cases, exposure to serotonin increased aphid mortality. To identify genes that are involved in serotonin biosynthesis, we conducted a transcriptome analysis and identified several predicted
S. viridis
tryptophan decarboxylase (
TDC
) and tryptamine 5-hydroxylase (
T5H
) genes. Two candidate genes were ectopically expressed in
Nicotiana tabacum,
where SvTDC1 (Sevir.6G066200) had tryptophan decarboxylase activity, and SvT5H1 (Sevir.8G219600) had tryptamine hydroxylase activity. Moreover, the function of the
SvTDC1
gene was validated using virus-induced gene silencing in
S. italica,
which caused a reduction in serotonin levels. This study provides the first evidence of serotonin biosynthesis in
Setaria
leaves. The biosynthesis of serotonin may play an important role in defense responses and could prove to be useful for developing more pest-tolerant
Setaria italica
cultivars.
The two-spotted spider mite (TSSM;
) is a ubiquitous polyphagous arthropod pest that has a major economic impact on the tomato (
) industry. Tomato plants have evolved broad defense mechanisms ...regulated by the expression of defense genes, phytohormones, and secondary metabolites present constitutively and/or induced upon infestation. Although tomato defense mechanisms have been studied for more than three decades, only a few studies have compared domesticated cultivars' natural mite resistance at the molecular level. The main goal of our research was to reveal the molecular differences between two tomato cultivars with similar physical (trichome morphology and density) and agronomic traits (fruit size, shape, color, cluster architecture), but with contrasting TSSM susceptibility. A net house experiment indicated a mite-resistance difference between the cultivars, and a climate-controlled performance and oviposition bioassay supported these findings. A transcriptome analysis of the two cultivars after 3 days of TSSM infestation, revealed changes in the genes associated with primary and secondary metabolism, including salicylic acid and volatile biosynthesis (volatile benzenoid ester and monoterpenes). The
genes,
, and
, encoding enzymes that synthesize the monoterpenes linalool, β-myrcene, limonene, and β-phellandrene were highly expressed in the resistant cultivar. The volatile profile of these cultivars upon mite infestation for 1, 3, 5, and 7 days, revealed substantial differences in monoterpenoid and phenylpropanoid volatiles, results consistent with the transcriptomic data. Comparing the metabolic changes that occurred in each cultivar and upon mite-infestation indicated that monoterpenes are the main metabolites that differ between cultivars (constitutive levels), while only minor changes occurred upon TSSM attack. To test the effect of these volatile variations on mites, we subjected both the TSSM and its corresponding predator,
, to an olfactory choice bioassay. The predator mites were only significantly attracted to the TSSM pre-infested resistant cultivar and not to the susceptible cultivar, while the TSSM itself showed no preference. Overall, our findings revealed the contribution of constitutive and inducible levels of volatiles on mite performance. This study highlights monoterpenoids' function in plant resistance to pests and may inform the development of new resistant tomato cultivars.
The shikimate pathway of plants mediates the conversion of primary carbon metabolites via chorismate into the three aromatic amino acids and to numerous secondary metabolites derived from them. ...However, the regulation of the shikimate pathway is still far from being understood. We hypothesized that 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DAHPS) is a key enzyme regulating flux through the shikimate pathway.
To test this hypothesis, we expressed a mutant bacterial AroG gene encoding a feedbackinsensitive DAHPS in transgenic Arabidopsis plants. The plants were subjected to detailed analysis of primary metabolism, using GC-MS, as well as secondary metabolism, using LCMS.
Our results exposed a major effect of bacterial AroG expression on the levels of shikimate intermediate metabolites, phenylalanine, tryptophan and broad classes of secondary metabolite, such as phenylpropanoids, glucosinolates, auxin and other hormone conjugates.
We propose that DAHPS is a key regulatory enzyme of the shikimate pathway. Moreover, our results shed light on additional potential metabolic bottlenecks bridging plant primary and secondary metabolism.
The aromatic amino acids phenylalanine, tyrosine, and tryptophan in plants are not only essential components of protein synthesis, but also serve as precursors for a wide range of secondary ...metabolites that are important for plant growth as well as for human nutrition and health. The aromatic amino acids are synthesized via the shikimate pathway followed by the branched aromatic amino acids biosynthesis pathway, with chorismate serving as a major intermediate branch point metabolite. Yet, the regulation and coordination of synthesis of these amino acids are still far from being understood. Recent studies on these pathways identified a number of alternative cross-regulated biosynthesis routes with unique evolutionary origins. Although the major route of Phe and Tyr biosynthesis in plants occurs via the intermediate metabolite arogenate, recent studies suggest that plants can also synthesize phenylalanine via the intermediate metabolite phenylpyruvate (PPY), similarly to many microorganisms. Recent studies also identified a number of transcription factors regulating the expression of genes encoding enzymes of the shikimate and aromatic amino acids pathways as well as of multiple secondary metabolites derived from them in Arabidopsis and in other plant species.
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