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Transcriptome profiling of low temperature-treated cassava apical shoots reveals dynamic responses of a tropical plant to cold stress

ABSTRACT: Background: Cassava is an important tropical root crop adapted to a wide range of environmental stimuli such as drought and acid soils. Nevertheless, it is an extremely cold-sensitive tropical species. Thus far, there is limited information about gene regulation and signaling pathways related to the cold stress response in cassava. The development of microarray technology has accelerated the study of global transcription profiling under certain conditions. Results: A 60-mer oligonucleotide 4X44K Agilent microarray representing 20,840 genes was used to perform transcriptome profiling in cassava apical shoots subjected to cold at 7°C for 0 h, 4 h, and 9 h. A total of 508 transcripts were identified as early cold-responsive genes in which 319 sequences had descriptions when they were aligned with Arabidopsis proteins. Gene ontology (GO) annotation analysis identified many interesting categories including ‘Response to abiotic and biotic stimulus’, ‘Response to stress’, ‘Transcription factor activity’, and ‘Chloroplast’. Various stress-associated genes comprising signal transduction components (e.g., MAP kinase 4), transcription factors (TFs; e.g., RAP2.11), and ROS scavenging enzymes (e.g., catalase 2), as well as photosynthesis-related genes (e.g., PSAL), were found. Seventeen major TF families were also identified as being involved in the early response to cold stress (e.g., AP2-EREBP). Meanwhile, KEGG pathway analysis uncovered many important pathways, including ‘Plant hormone signal transduction’, ‘Starch and sucrose metabolism’, and ‘Plant-pathogen interaction’. Furthermore, the expression changes of 18 genes under cold and other abiotic stresses conditions were validated by real-time RT-PCR. As a response to cold stress in cassava, an increase in the ROS scavenging enzyme activities of catalase and superoxide dismutases and the accumulation of total soluble sugars were also detected. Importantly, most of the tested stress-responsive genes were primarily expressed in mature leaves, stem cambia, and fibrous roots rather than apical buds and young leaves. Conclusions: The dynamic expression changes reflect the integrative controlling and transcriptome regulation of the networks in the early cold stress response of cassava. The biological processes involved in the signal perception and physiological response might shed light on the molecular mechanisms related to cold tolerance in tropical plants and provide useful candidate genes for genetic improvement.

ORGANISM(S): Manihot esculenta

PROVIDER: GSE31073 | GEO | 2013/01/17

SECONDARY ACCESSION(S): PRJNA144715

REPOSITORIES: GEO

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Project description:Background: Cassava is an important tropical root crop adapted to a wide range of environmental stimuli such as drought and acid soils. Nevertheless, it is an extremely cold-sensitive tropical species. Thus far, there is limited information about gene regulation and signaling pathways related to the cold stress response in cassava. The development of microarray technology has accelerated the study of global transcription profiling under certain conditions. Results: A 60-mer oligonucleotide 4X44K Agilent microarray representing 20,840 genes was used to perform transcriptome profiling in cassava apical shoots subjected to cold at 7M-BM-0C for 0 h, 4 h, and 9 h. A total of 508 transcripts were identified as early cold-responsive genes in which 319 sequences had descriptions when they were aligned with Arabidopsis proteins. Gene ontology (GO) annotation analysis identified many interesting categories including M-bM-^@M-^XResponse to abiotic and biotic stimulusM-bM-^@M-^Y, M-bM-^@M-^XResponse to stressM-bM-^@M-^Y, M-bM-^@M-^XTranscription factor activityM-bM-^@M-^Y, and M-bM-^@M-^XChloroplastM-bM-^@M-^Y. Various stress-associated genes comprising signal transduction components (e.g., MAP kinase 4), transcription factors (TFs; e.g., RAP2.11), and ROS scavenging enzymes (e.g., catalase 2), as well as photosynthesis-related genes (e.g., PSAL), were found. Seventeen major TF families were also identified as being involved in the early response to cold stress (e.g., AP2-EREBP). Meanwhile, KEGG pathway analysis uncovered many important pathways, including M-bM-^@M-^XPlant hormone signal transductionM-bM-^@M-^Y, M-bM-^@M-^XStarch and sucrose metabolismM-bM-^@M-^Y, and M-bM-^@M-^XPlant-pathogen interactionM-bM-^@M-^Y. Furthermore, the expression changes of 18 genes under cold and other abiotic stresses conditions were validated by real-time RT-PCR. As a response to cold stress in cassava, an increase in the ROS scavenging enzyme activities of catalase and superoxide dismutases and the accumulation of total soluble sugars were also detected. Importantly, most of the tested stress-responsive genes were primarily expressed in mature leaves, stem cambia, and fibrous roots rather than apical buds and young leaves. Conclusions: The dynamic expression changes reflect the integrative controlling and transcriptome regulation of the networks in the early cold stress response of cassava. The biological processes involved in the signal perception and physiological response might shed light on the molecular mechanisms related to cold tolerance in tropical plants and provide useful candidate genes for genetic improvement. Apical shoots subjected to cold at 7M-BM-0C for 0 h, 4 h, and 9 h were collected for RNA extractions from three independent healthy 3-month-old cassava (cultivar TMS60444) plants in the greenhouse.

Project description:Stress acclimation is an effective mechanism that plants acquired for adaption to dynamic environmental conditions. After undergoing cold acclimation, plants become more tolerant to cold stress. In order to understand the mechanism of cold acclimation, we performed a systematic, comprehensive study of cold response and acclimation in Cassava (Manihot esculenta), a staple crop and major food source in the tropical regions of the world. We profiled mRNA genes and small-RNA species, using next generation sequencing, and performed an integrative analysis of the transcriptome and microRNAome of Cassava across the normal condition, a moderate cold stress at 14M-BM-0C, a harsh stress at 4M-BM-0C after cold acclimation at 14M-BM-0C, and a cold shock from 24M-BM-0C to 4M-BM-0C. Two results from the analysis were striking. First, the moderate stress and cold shock, despite a difference of 10M-BM-0C between the two, triggered comparable degrees of perturbation to the transcriptome; in contrary, further harsh stress after cold acclimation resulted in a much smaller degree of transcriptome variation. Second and more importantly, about two thirds of the up- or down-regulated genes after moderate stress reversed their expression to down- or up-regulation, respectively, under harsh stress after cold acclimation, resulting in a genome-wide rewiring of regulatory networks. MicroRNAs, which are key post-transcriptional gene regulators, were major players in this massive rewiring of genetic circuitry. Further, a function enrichment analysis of the perturbed genes revealed that cold acclimation helped the plant to develop immunity to further harsh stress by exclusively inducing genes with functions of nutrient reservoir; in contrast, many genes with functions of viral reproduction were induced by cold shock. Our study revealed, for the first time, the molecular basis of stress acclimation in plants, and shed lights on the role of microRNA gene regulation in cold response and acclimation in Euphorbia. Three organs/tissues (folded leaf, fully expanded leaf and roots) of Cassava cultivar SC124 harvested at 6h, 24h and 5d for three cold treatments of CA, CCA and CS, for gene expression profiling at the stages of initial response, secondary response, and functional adaption to cold stresses. Total RNA of each sample was isolated individually, and then pooled with an equal amount from each sample into one for profiling. As a result, four mRNA libraries and four small-RNA libraries, corresponding to the conditions of CA, CCA, CS and NC, were constructed.

Project description:Stress acclimation is an effective mechanism that plants acquired for adaption to dynamic environmental conditions. After undergoing cold acclimation, plants become more tolerant to cold stress. In order to understand the mechanism of cold acclimation, we performed a systematic, comprehensive study of cold response and acclimation in Cassava (Manihot esculenta), a staple crop and major food source in the tropical regions of the world. We profiled mRNA genes and small-RNA species, using next generation sequencing, and performed an integrative analysis of the transcriptome and microRNAome of Cassava across the normal condition, a moderate cold stress at 14°C, a harsh stress at 4°C after cold acclimation at 14°C, and a cold shock from 24°C to 4°C. Two results from the analysis were striking. First, the moderate stress and cold shock, despite a difference of 10°C between the two, triggered comparable degrees of perturbation to the transcriptome; in contrary, further harsh stress after cold acclimation resulted in a much smaller degree of transcriptome variation. Second and more importantly, about two thirds of the up- or down-regulated genes after moderate stress reversed their expression to down- or up-regulation, respectively, under harsh stress after cold acclimation, resulting in a genome-wide rewiring of regulatory networks. MicroRNAs, which are key post-transcriptional gene regulators, were major players in this massive rewiring of genetic circuitry. Further, a function enrichment analysis of the perturbed genes revealed that cold acclimation helped the plant to develop immunity to further harsh stress by exclusively inducing genes with functions of nutrient reservoir; in contrast, many genes with functions of viral reproduction were induced by cold shock. Our study revealed, for the first time, the molecular basis of stress acclimation in plants, and shed lights on the role of microRNA gene regulation in cold response and acclimation in Euphorbia.

Project description:Rice in tropical and sub-tropical areas is often subjected to cold stress at the seedling stage resulting in poor growth and yield loss. In general, japonica rice has stronger cold tolerance (CT) than indica rice. However, several favorite alleles for CT exist in indica rice and can be used to enhance CT under japonica background. Genome-wide gene expression profiling is the efficient way to decipher the molecular genetic mechanism of CT enhancement and provide valuable information for the CT improvement in rice molecular breeding. In this study, the transcriptome of a CT introgressed line (IL) K354 and its recurrent parent C418 under cold stress were comparatively analyzed to explore the possible CT enhancement mechanism of K354.Totally 3184 differentially expressed genes (DEGs) including 195 transcription factors were identified in both lines under cold stress, about half of them were commonly regulated, which were involved in the major cold responsive pathways including OsDREB1s regulon. The K354-specific cold-induced DEGs were mainly related to stimulus response, cellular cell wall organization, and microtubule-based movement process compared with commonly cold-induced DEGs by GO analysis. Moreover, 296 constitutive DEGs with significantly different transcription level between C418 and K354 were detected under both control and cold stress conditions. K354-specific cold-regulated and constitutive DEGs jointly account for the CT improvement of K354. Pathway analysis unraveled up-regulation of starch and sucrose metabolism in both genotypes and presumably weaker defense response to stress in K354 than C418 under cold stress. Candidate genes prediction based on previous putative CT genetic networks revealed genotype-dependent CT enhancement mechanism in CT IL K354 vs recurrent parent C418, including Sir2, OsFAD7, OsWAK112d, and PCD related genes, etc.We propose a hypothesis of the CT enhancement mechanism in rice based on the results in present study. Firstly, a number of cold-regulated genes are able to express constitutively at high level or absent under control condition for standing by the arrival of cold stress. Next, under cold stress slower perception of stress signal from the more cold-tolerant membrane can postpone the activation of defensive system which may have possible negative effects on rice growth. Then, PCD will be launched to sacrifice a few cells for maintaining the basal growth of most cells. Finally, the protective responses on multiple aspects of cold damage will be postponed because of delayed several cold-defensive pathways (i.e. OsDREB1C regulon). It might explain why the recovery capacity of K354 from cold stress to control condition is stronger than C418. The CT enhancement mechanism can be regarded as the possible way to improve CT of japonica rice using indica germplasm in rice breeding program. In this study, the specific gene expression patterns of two genotypes (C418 and K354) at 2h, 6h, 12h, 24h and 48h during cold stress treatment (4 C) and control were characterized by using the Affymetrix rice microarray platform.

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Transcriptome profiling of low temperature-treated cassava apical shoots reveals dynamic responses of a tropical plant to cold stress

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