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Concurrent Drought Stress and Vascular Pathogen Infection Induce Common and Distinct Transcriptomic Responses in Chickpea.

ABSTRACT: Chickpea (Cicer arietinum); the second largest legume grown worldwide is prone to drought and various pathogen infections. These drought and pathogen stresses often occur concurrently in the field conditions. However, the molecular events in response to that are largely unknown. The present study examines the transcriptome dynamics in chickpea plants exposed to a combination of water-deficit stress and Ralstonia solanacearum infection. R. solanacearum is a potential wilt disease causing pathogen in chickpea. Drought stressed chickpea plants were infected with this pathogen and the plants were allowed to experience progressive drought with 2 and 4 days of R. solanacearum infection called short duration stress (SD stresses) and long duration stress (LD stresses), respectively. Our study showed that R. solanacearum multiplication decreased under SD-combined stress compared to SD-pathogen but there was no significant change in LD-combined stress compared to LD-pathogen. The microarray analysis during these conditions showed that 821 and 1039 differentially expressed genes (DEGs) were unique to SD- and LD-combined stresses, respectively, when compared with individual stress conditions. Three and fifteen genes were common among all the SD-stress treatments and LD-stress treatments, respectively. Genes involved in secondary cell wall biosynthesis, alkaloid biosynthesis, defense related proteins, and osmo-protectants were up-regulated during combined stress. The expression of genes involved in lignin and cellulose biosynthesis were specifically up-regulated in SD-combined, LD-combined, and LD-pathogen stress. A close transcriptomic association of LD-pathogen stress with SD-combined stress was observed in this study which indicates that R. solanacearum infection also exerts drought stress along with pathogen stress thus mimics combined stress effect. Furthermore the expression profiling of candidate genes using real-time quantitative PCR validated the microarray data. The study showed that down-regulation of defense-related genes during LD-combined stress resulted in an increased bacterial multiplication as compared to SD-combined stress. Overall, our study highlights a sub-set of DEGs uniquely expressed in response to combined stress, which serve as potential candidates for further functional characterization to delineate the molecular response of the plant to concurrent drought-pathogen stress.

SUBMITTER: Sinha R

PROVIDER: S-EPMC5361651 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Concurrent Drought Stress and Vascular Pathogen Infection Induce Common and Distinct Transcriptomic Responses in Chickpea.

Sinha Ranjita R Gupta Aarti A Senthil-Kumar Muthappa M

Frontiers in plant science 20170314

Chickpea (Cicer arietinum); the second largest legume grown worldwide is prone to drought and various pathogen infections. These drought and pathogen stresses often occur concurrently in the field conditions. However, the molecular events in response to that are largely unknown. The present study examines the transcriptome dynamics in chickpea plants exposed to a combination of water-deficit stress and Ralstonia solanacearum infection. R. solanacearum is a potential wilt dis ...[more]

PMID: 28382041

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Project description:‘Pulsechip’, a boutique cDNA microarray, generated from a set of chickpea (Cicer arietinum L.) unigenes, grasspea (Lathyrus sativus L.) ESTs and lentil (Lens culinaris Med.) resistance gene analogs, was employed to generate an expression profile of chickpea accessions tolerant and susceptible to drought stress. Two groups of a tolerant and susceptible accession were challenged with drought stress. The experiments were performed in three biological replications. The experiments were conducted in reference design where respective tissues from unstressed plants served as control. The leaf and flower/bud tissues were collected and used for hybridization to measure changes in RNA abundance of treatment vs. control. The tissues from five experimental replicate plants per biological replication were pooled together (leaf and flower tissues separate) before RNA extraction. This RNA was used to prepare cDNA targets for expression analysis using microarray. The microarray had six technical replicate spots per EST. The transcript level for each EST/cDNA was firstly calculated as the average intensity of the six technical replicates and then the average intensity of three biological replicates. Data analysis included LOWESS normalization (LOcally WEighted polynomial regreSSion) to adjust for differences in quantity of initial RNA, labeling and detection efficiencies. A dye swap in one biological replicate adjusted dye bias, if any. The Differentially Expressed (DE) ESTs were identified as those with a 95% confidence interval for mean fold change (FC) that extended beyond the two-fold cut-off and also passed the Students t test (P<0.05) and FDR correction. These cut-offs translate into induced ESTs having a log2 ratio > 1 and repressed ESTs a ratio of < -1. The analysis consisted of three fold comparison. Firstly, the ESTs that were differentially expressed between treatment and control plants of each accession were detected. Then the ESTs that were similarly expressed by tolerant and susceptible accessions were then eliminated by comparison. This included a two-way comparison, where tolerant and susceptible genotypes were compared within and between groups. Lastly, ESTs that were consensually differentially expressed between tolerant and susceptible accessions of the two batches were identified. The hypothesis was that if a putative gene was consistently expressed only in tolerant or susceptible genotype for a particular stress, it might be a candidate for tolerance/susceptibility for that stress. Globally, the level of 114 transcripts was affected in response to drought stress in all the genotypes and tissue types studied. The DE transcripts in response to drought stress coded for various functional and regulatory proteins, most of which were repressed. Protein and other solute transport was repressed in susceptible-1 flowers but induced in tolerant-2 flowers, as evidenced by the induction of a protein-transport facilitation protein (DY475074) in flowers of tolerant-2 and repression of a aquaporin-like membrane channel protein (DY396334) and DNA-J like protein involved in intracellular protein transport (DY475488) in flowers of susceptible-1. Two putative auxin-repressed proteins (DY396289, DY396359) were highly repressed in flowers and leaves of tolerant-2, whilst being induced in flowers and leaves of susceptible-1. Defence-related genes including pathogenesis-related proteins (DY396305 and DY396343), nematode-resistance protein (CV793603), Cf-9 gene cluster (DY396352) and disease resistance response proteins (DY396265 and DY396276) were repressed in flowers of tolerant and susceptible genotypes. A Pea (pi230) disease resistance response protein (DY396390) and a multi-resistance protein ABC transporter (CV793605) were induced in flowers of both tolerant genotypes. Some genes involved in energy metabolism (DY396279 and DY475316) were repressed in leaves and flowers of tolerant and susceptible genotypes. Additionally, some transcripts related to senescence, including auxin responsive protein IAA9 (DY396315), senescence-associated protein DIN 1 (DY396338), and dehydration stress-induced protein (DY396321) were repressed in leaves and flowers of the tolerant genotypes. Of the 114 DE transcripts expressed in drought tolerant and susceptible genotypes, only two were consistently expressed. These included a cytosolic fructose 1,6-bisphosphatase (DY475548) and a gene with unknown function, which were repressed in flowers of both susceptible genotypes. Keywords: Chickpea, Drought stress, Tolerant, Susceptible, cDNA microarray

Project description:In field conditions, plants are concurrently exposed to multiple stresses, where one stressor impacts the plant's response to another stressor, and the resultant net effect of these stresses differs from individual stress response. The present study investigated the effect of drought stress on interaction of chickpea with Pseudomonas syringae pv. phaseolicola (Psp; foliar pathogen) and Ralstonia solanacearum (Rs; xylem inhabiting wilt causing pathogen), respectively, and the net-effect of combined stress on chlorophyll content and cell death. Two type of stress treatments were used to study the influence of each stress factor during combined stress, viz., imposition of drought stress followed by pathogen challenge (DP), and pathogen inoculated plants imposed with drought in course of pathogen infection (PD). Drought stress was imposed at different levels with pathogen inoculum to understand the influence of different stress intensities on stress interaction and their net impact. Drought stressed chickpea plants challenged with Psp infection (DPsp) showed reduced in planta bacterial number compared to Psp infection alone. Similarly, Rs infection of chickpea plants showed reduced in planta bacterial number under severe drought stress. Combined drought and Psp (DPsp) infected plants showed decreased cell death compared to plants infected only with Psp but the extent of cell death was similar to drought stressed plants. Similarly, chlorophyll content in plants under combined stress was similar to the individual drought stressed plants; however, the chlorophyll content was more compared to pathogen only infected plants. Under combined drought and Rs infection (DRs), cell death was similar to individual drought stress but significantly less compared to only Rs infected plants. Altogether, the study proposes that both stress interaction and net effect of combined stress could be majorly influenced by first occurring stress, for example, drought stress in DP treatment. In addition, our results indicate that the outcome of the two stress interaction in plant depends on timing of stress occurrence and nature of infecting pathogen.

Project description:The present study aimed at identifying and mapping key genes expressed in root tissues involved in drought and salinity tolerance/resistance conserved among different fruit tree species. Twenty-six RNA-Seq samples were analyzed from six published studies in five plant species (Olea europaea, Vitis riparia Michx, Prunus mahaleb, Prunus persica, Phoenix dactylifera). This meta-analysis used a bioinformatic pipeline identifying 750 genes that were commonly modulated in three salinity studies and 683 genes that were commonly regulated among three drought studies, implying their conserved role in resistance/tolerance/response to these environmental stresses. A comparison was done on the genes that were in common among both salinity and drought resulted in 82 genes, of which 39 were commonly regulated with the same trend of expression (23 were upregulated and 16 were downregulated). Gene set enrichment and pathway analysis pointed out that pathways encoding regulation of defense response, drug transmembrane transport, and metal ion binding are general key molecular responses to these two abiotic stress responses. Furthermore, hormonal molecular crosstalk plays an essential role in the fine-tuning of plant responses to drought and salinity. Drought and salinity induced a different molecular "hormonal fingerprint". Dehydration stress specifically enhanced multiple genes responsive to abscisic acid, gibberellin, brassinosteroids, and the ethylene-activated signaling pathway. Salt stress mostly repressed genes encoding for key enzymes in signaling proteins in auxin-, gibberellin-(gibberellin 2 oxidase 8), and abscisic acid-related pathways (aldehyde oxidase 4, abscisic acid-responsive element-binding protein 3). Abiotic stress-related genes were mapped into the chromosome to identify molecular markers usable for the improvement of these complex quantitative traits. This meta-analysis identified genes that serve as potential targets to develop cultivars with enhanced drought and salinity resistance and/or tolerance across different fruit tree crops in a biotechnological sustainable way.

Project description:BackgroundPolygonatum kingianum Coll. et Hemsl. is an important plant in Traditional Chinese Medicine. The extracts from its tubers are rich in polysaccharides and other metabolites such as saponins. It is a well-known concept that growing medicinal plants in semi-arid (or drought stress) increases their natural compounds concentrations. This study was conducted to explore the morpho-physiological responses of P. kingianum plants and transcriptomic signatures of P. kingianum tubers exposed to mild, moderate, and severe drought and rewatering.ResultsThe stress effects on the morpho-physiological parameters were dependent on the intensity of the drought stress. The leaf area, relative water content, chlorophyll content, and shoot fresh weight decreased whereas electrolyte leakage increased with increase in drought stress intensity. A total of 53,081 unigenes were obtained; 59% of which were annotated. We observed that 1352 and 350 core genes were differentially expressed in drought and rewatering, respectively. Drought stress driven differentially expressed genes (DEGs) were enriched in phenylpropanoid biosynthesis, flavonoid biosynthesis, starch and sucrose metabolism, and stilbenoid diarylheptanoid and gingerol biosynthesis, and carotenoid biosynthesis pathways. Pathways such as plant-pathogen interaction and galactose metabolism were differentially regulated between severe drought and rewatering. Drought reduced the expression of lignin, gingerol, and flavonoid biosynthesis related genes and rewatering recovered the tubers from stress by increasing the expression of the genes. Increased expression of carotenoid biosynthesis pathway related genes under drought suggested their important role in stress endurance. An increase in starch and sucrose biosynthesis was evident from transcriptomic changes under drought stress. Rewatering recovered the drought affected tubers as evident from the contrasting expression profiles of genes related to these pathways. P. kingianum tuber experiences an increased biosynthesis of sucrose, starch, and carotenoid under drought stress. Drought decreases the flavonoids, phenylpropanoids, gingerol, and lignin biosynthesis. These changes can be reversed by rewatering the P. kingianum plants.ConclusionsThese results provide a transcriptome resource for P. kingianum and expands the knowledge on the effect of drought and rewatering on important pathways. This study also provides a large number of candidate genes that could be manipulated for drought stress tolerance and managing the polysaccharide and secondary metabolites' contents in P. kingianum.

Project description:‘Pulsechip’, a boutique cDNA microarray, generated from a set of chickpea (Cicer arietinum L.) unigenes, grasspea (Lathyrus sativus L.) ESTs and lentil (Lens culinaris Med.) resistance gene analogs, was employed to generate an expression profile of chickpea genotype ICC 3996 to drought, cold and high-salinity stresses. The experiments were performed in three biological replications. The experiments were conducted in reference design where respective tissues from unstressed plants served as control. The leaf/shoot, flower/pod and/or root tissues were collected and used for hybridization to measure changes in RNA abundance of treatment vs. control. The tissues from five experimental replicate plants per biological replication were pooled together (leaf/flower/root tissues pooled separately) before RNA extraction. This RNA was used to prepare cDNA targets for expression analysis using microarray. The microarray had six technical replicate spots per EST. The transcript level for each EST/cDNA was firstly calculated as the average intensity of the six technical replicates and then the average intensity of three biological replicates. Data analysis included LOWESS normalization (LOcally WEighted polynomial regreSSion) to adjust for differences in quantity of initial RNA, labeling and detection efficiencies. A dye swap in one biological replicate adjusted dye bias, if any. The Differentially Expressed (DE) ESTs were identified as those with a 95% confidence interval for mean fold change (FC) that extended beyond the two-fold cut-off and also passed the Students t test (P<0.05) and FDR correction. These cut-offs translate into induced ESTs having a log2 ratio > 1 and repressed ESTs a ratio of < -1. Overall, 46, 54 and 266 ESTs were identified as DE under drought, cold, and high-salinity stresses, respectively. The important ones DE in response to drought stress include induction of transcripts associated with dehydrin-cognate, lipid-transfer protein precursor, and glutamate-hydrolysing asparagine synthetase, whilst repression of transcripts associated with senescence, photosynthesis/energy metabolism, auxin-repressed protein, starch metabolism, AP2/EREBP1 DNA binding domain, putative ARF1 GTPase activating protein, and histidine-containing phosphotransfer protein ATHP3. The interesting transcripts DE in response to cold-stress included induction of phosphate-induced protein, cationic peroxidase, UDP-glucose 4-epimerase, Avr9/Cf9 rapidly elicited protein, DNA-J like protein involved in intracellular protein transport, and protein kinase, whist repression of transcripts associated with a hypothetical transmembrane protein, membrane related protein CP5, lipid-transfer protein precursor, WD repeat protein and several transcripts associated with cellular metabolism, cell cycle and DNA processing, protein synthesis and photosynthesis/energy metabolism. Under high-salinity stress, several transcripts were DE only in roots at 24 hpt but DE in shoots or both, shoots and roots at 48 hpt, relating to the theory of upward movement of salt to shoots at later stages when roots fail to restrict it (Munns et al., 2002). The important transcripts DE in response to high-salinity stress included induction of aluminum-induced protein, auxin-repressed proteins, metallothionein-like protein, glutamate dehydrogenase, sucrose synthase, UDP-glucose 4-epimerase, xylose isomerase, class 10 pathogenesis related protein, disease resistance protein, SNAKIN 2 antimicrobial peptide, and DNA-J like protein involved in intra-cellular protein transport. Whilst high-salinity stress caused the repression of transcripts associated with cell rescue/death, cell cycle/DNA processing, cellular metabolism, photosynthesis/energy metabolism, and transport facilitation. Several of the above transcripts have been previously implicated to be associated with abiotic stress response in other crops. Hence, the study of more genotypes and transcriptional changes at several time points may provide a better picture of involvement of the genes being interrogated here in drought tolerance/susceptibility. Subsequently, the functionality of candidate tolerance genes detected through this approach could be validated by overexpressing the genes through transgenics or silencing them using knockout-mutants/antisense/RNAi. Keywords: abiotic stress response, drought, cold, high-salinity, chickpea

Project description:To obtain an insight into host-pathogen interactions in clostridial myonecrosis, we carried out comparative transcriptome analysis of both the bacterium and the host in a murine Clostridium perfringens infection model, which is the first time that such an investigation has been conducted. Analysis of the host transcriptome from infected muscle tissues indicated that many genes were upregulated compared to the results seen with mock-infected mice. These genes were enriched for host defense pathways, including Toll-like receptor (TLR) and Nod-like receptor (NLR) signaling components. Real-time PCR confirmed that host TLR2 and NLRP3 inflammasome genes were induced in response to C. perfringens infection. Comparison of the transcriptome of C. perfringens cells from the infected tissues with that from broth cultures showed that host selective pressure induced a global change in C. perfringens gene expression. A total of 33% (923) of C. perfringens genes were differentially regulated, including 10 potential virulence genes that were upregulated relative to their expression in vitro These genes encoded putative proteins that may be involved in the synthesis of cell wall-associated macromolecules, in adhesion to host cells, or in protection from host cationic antimicrobial peptides. This report presents the first successful expression profiling of coregulated transcriptomes of bacterial and host genes during a clostridial myonecrosis infection and provides new insights into disease pathogenesis and host-pathogen interactions.IMPORTANCEClostridium perfringens is the causative agent of traumatic clostridial myonecrosis, or gas gangrene. In this study, we carried out transcriptional analysis of both the host and the bacterial pathogen in a mouse myonecrosis infection. The results showed that in comparison to mock-infected control tissues, muscle tissues from C. perfringens-infected mice had a significantly altered gene expression profile. In particular, the expression of many genes involved in the innate immune system was upregulated. Comparison of the expression profiles of C. perfringens cells isolated from the infected tissues with those from equivalent broth cultures identified many potential virulence genes that were significantly upregulated in vivo These studies have provided a new understanding of the range of factors involved in host-pathogen interactions in a myonecrosis infection.

Dataset Information

Concurrent Drought Stress and Vascular Pathogen Infection Induce Common and Distinct Transcriptomic Responses in Chickpea.

Publications

Concurrent Drought Stress and Vascular Pathogen Infection Induce Common and Distinct Transcriptomic Responses in Chickpea.

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