Transcriptome Analysis Reveals Key Cold-Stress-Responsive Genes in Winter Rapeseed (Brassica rapa L.)

Low ambient air temperature limits the growth and selection of crops in cold regions, and cold tolerance is a survival strategy for overwintering plants in cold winters. Studies of differences in transcriptional levels of winter rapeseed (Brassica rapa L.) under cold stress can improve our understanding of transcript-mediated cold stress responses. In this study, two winter rapeseed varieties, Longyou-7 (cold-tolerant) and Lenox (cold-sensitive), were used to reveal morphological, physiological, and transcriptome levels after 24 h of cold stress, and 24 h at room temperature, to identify the mechanism of tolerance to cold stress. Compared to Lenox, Longyou-7 has a shorter growth period and greater belowground mass, and exhibits stronger physiological activity after cold stress. Subsequently, more complete genomic annotation was obtained by sequencing. A total of 10,251 and 10,972 differentially expressed genes (DEG) were identified in Longyou-7 and Lenox, respectively. Six terms closely related to cold stress were found by the Gene Ontology (GO) function annotation. Some of these terms had greater upregulated expression in Longyou-7, and the expression of these genes was verified by qRT-PCR. Most of these DEGs are involved in phenylpropanoid biosynthesis, plant hormone signal transduction, ribosome biogenesis, MAPK signaling pathway, basal transcription factors, and photosynthesis. Analysis of the genes involved in the peroxisome pathway revealed that Longyou-7 and Lenox may have different metabolic patterns. Some transcription factors may play an important role in winter rapeseed tolerance to cold stress, and Longyou-7 is slightly slower than Lenox. Our results provide a transcriptome database and candidate genes for further study of winter rapeseed cold stress.

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iTRAQ-based quantitative proteome analysis insights into cold stress of Winter Rapeseed (Brassica rapa L.) grown in the field

Scientific Reports ◽

10.1038/s41598-021-02707-z ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Zaoxia Niu ◽

Lijun Liu ◽

Yuanyuan Pu ◽

Li Ma ◽

Junyan Wu ◽

...

Keyword(s):

Cold Stress ◽

Brassica Rapa ◽

Molecular Mechanisms ◽

Glutathione Transferase ◽

Soluble Sugars ◽

Freezing Stress ◽

Transferase Activity ◽

Oilseed Crop ◽

Winter Rapeseed ◽

Collar Diameter

AbstractWinter rapeseed (Brassica rapa L.) is a major oilseed crop in Northern China, where its production was severely affected by chilling and freezing stress. However, not much is known about the role of differentially accumulated proteins (DAPs) during the chilling and freezing stress. In this study, isobaric tag for relative and absolute quantification (iTRAQ) technology was performed to identify DAPs under freezing stress. To explore the molecular mechanisms of cold stress tolerance at the cellular and protein levels, the morphological and physiological differences in the shoot apical meristem (SAM) of two winter rapeseed varieties, Longyou 7 (cold-tolerant) and Lenox (cold-sensitive), were explored in field-grown plants. Compared to Lenox, Longyou 7 had a lower SAM height and higher collar diameter. The level of malondialdehyde (MDA) and indole-3-acetic acid (IAA) content was also decreased. Simultaneously, the soluble sugars (SS) content, superoxide dismutase (SOD) activity, peroxidase (POD) activity, soluble protein (SP) content, and collar diameter were increased in Longyou 7 as compared to Lenox. A total of 6330 proteins were identified. Among this, 98, 107, 183 and 111 DAPs were expressed in L7 CK/Le CK, L7 d/Le d, Le d/Le CK and L7 d/L7 CK, respectively. Quantitative real-time PCR (RT-qPCR) analysis of the coding genes for seventeen randomly selected DAPs was performed for validation. These DAPs were identified based on gene ontology enrichment analysis, which revealed that glutathione transferase activity, carbohydrate-binding, glutathione binding, metabolic process, and IAA response were closely associated with the cold stress response. In addition, some cold-induced proteins, such as glutathione S-transferase phi 2(GSTF2), might play an essential role during cold acclimation in the SAM of Brassica rapa. The present study provides valuable information on the involvement of DAPs during cold stress responses in Brassica rapa L, and hence could be used for breeding experiments.

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Golgi stress–induced transcriptional changes mediated by MAPK signaling and three ETS transcription factors regulate MCL1 splicing

Molecular Biology of the Cell ◽

10.1091/mbc.e17-06-0418 ◽

2018 ◽

Vol 29 (1) ◽

pp. 42-52 ◽

Cited By ~ 13

Author(s):

Jan Baumann ◽

Tatiana I. Ignashkova ◽

Sridhar R. Chirasani ◽

Silvia Ramírez-Peinado ◽

Hamed Alborzinia ◽

...

Keyword(s):

Transcription Factors ◽

Stress Responses ◽

Secretory Pathway ◽

Target Genes ◽

Enrichment Analysis ◽

Mapk Signaling ◽

Gene Set Enrichment Analysis ◽

Loss Of Function ◽

Control Of Gene Expression ◽

Ets Family

The secretory pathway is a major determinant of cellular homoeostasis. While research into secretory stress signaling has so far mostly focused on the endoplasmic reticulum (ER), emerging data suggest that the Golgi itself serves as an important signaling hub capable of initiating stress responses. To systematically identify novel Golgi stress mediators, we performed a transcriptomic analysis of cells exposed to three different pharmacological compounds known to elicit Golgi fragmentation: brefeldin A, golgicide A, and monensin. Subsequent gene-set enrichment analysis revealed a significant contribution of the ETS family transcription factors ELK1, GABPA/B, and ETS1 to the control of gene expression following compound treatment. Induction of Golgi stress leads to a late activation of the ETS upstream kinases MEK1/2 and ERK1/2, resulting in enhanced ETS factor activity and the transcription of ETS family target genes related to spliceosome function and cell death induction via alternate MCL1 splicing. Further genetic analyses using loss-of-function and gain-of-function experiments suggest that these transcription factors operate in parallel.

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Genome-Wide Identification and Characterization of bZIP Transcription Factors inBrassica oleraceaunder Cold Stress

BioMed Research International ◽

10.1155/2016/4376598 ◽

2016 ◽

Vol 2016 ◽

pp. 1-18 ◽

Cited By ~ 4

Author(s):

Indeok Hwang ◽

Ranjith Kumar Manoharan ◽

Jong-Goo Kang ◽

Mi-Young Chung ◽

Young-Wook Kim ◽

...

Keyword(s):

Transcription Factors ◽

Amino Acid ◽

Cold Stress ◽

Stress Responses ◽

Sequence Similarity ◽

Amino Acid Sequences ◽

Amino Acid Sequence Similarity ◽

Sequencing Data ◽

Cold Response ◽

Bzip Transcription Factors

Cabbages (Brassica oleraceaL.) are an important vegetable crop around world, and cold temperature is among the most significant abiotic stresses causing agricultural losses, especially in cabbage crops. Plant bZIP transcription factors play diverse roles in biotic/abiotic stress responses. In this study, 119 putative BolbZIP transcription factors were identified using amino acid sequences from several bZIP domain consensus sequences. The BolbZIP members were classified into 63 categories based on amino acid sequence similarity and were also compared with BrbZIP and AtbZIP transcription factors. Based on this BolbZIP identification and classification, cold stress-responsiveBolbZIPgenes were screened in inbred lines,BN106andBN107, using RNA sequencing data and qRT-PCR. The expression level of the 3 genes,Bol008071,Bol033132, andBol042729, was significantly increased inBN107under cold conditions and was unchanged inBN106. The upregulation of these genes inBN107, a cold-susceptible inbred line, suggests that they might be significant components in the cold response. Among three identified genes,Bol033132has 97% sequence similarity toBra020735, which was identified in a screen for cold-related genes inB. rapaand a protein containing N-rich regions in LCRs. The results obtained in this study provide valuable information for understanding the potential function of BolbZIP transcription factors in cold stress responses.

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Transcriptome analysis of newly classified bZIP transcription factors of Brassica rapa in cold stress response

Genomics ◽

10.1016/j.ygeno.2014.07.008 ◽

2014 ◽

Vol 104 (3) ◽

pp. 194-202 ◽

Cited By ~ 20

Author(s):

Indeok Hwang ◽

Hee-Jeong Jung ◽

Jong-In Park ◽

Tae-Jin Yang ◽

Ill-Sup Nou

Keyword(s):

Transcription Factors ◽

Stress Response ◽

Cold Stress ◽

Brassica Rapa ◽

Transcriptome Analysis ◽

Bzip Transcription Factors

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Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression

Journal of Experimental Botany ◽

10.1093/jxb/erz261 ◽

2019 ◽

Vol 70 (19) ◽

pp. 5355-5374 ◽

Cited By ~ 11

Author(s):

Dandan Zang ◽

Jingxin Wang ◽

Xin Zhang ◽

Zhujun Liu ◽

Yucheng Wang

Keyword(s):

Gene Expression ◽

Transcription Factors ◽

Heat Shock ◽

Salt Tolerance ◽

Stress Responses ◽

Ion Homeostasis ◽

Cellulose Synthase ◽

Regulate Gene Expression ◽

E Box ◽

Regulate Gene

Abstract Plant heat shock transcription factors (HSFs) are involved in heat and other abiotic stress responses. However, their functions in salt tolerance are little known. In this study, we characterized the function of a HSF from Arabidopsis, AtHSFA7b, in salt tolerance. AtHSFA7b is a nuclear protein with transactivation activity. ChIP-seq combined with an RNA-seq assay indicated that AtHSFA7b preferentially binds to a novel cis-acting element, termed the E-box-like motif, to regulate gene expression; it also binds to the heat shock element motif. Under salt conditions, AtHSFA7b regulates its target genes to mediate serial physiological changes, including maintaining cellular ion homeostasis, reducing water loss rate, decreasing reactive oxygen species accumulation, and adjusting osmotic potential, which ultimately leads to improved salt tolerance. Additionally, most cellulose synthase-like (CSL) and cellulose synthase (CESA) family genes were inhibited by AtHSFA7b; some of them were randomly selected for salt tolerance characterization, and they were mainly found to negatively modulate salt tolerance. By contrast, some transcription factors (TFs) were induced by AtHSFA7b; among them, we randomly identified six TFs that positively regulate salt tolerance. Thus, AtHSFA7b serves as a transactivator that positively mediates salinity tolerance mainly through binding to the E-box-like motif to regulate gene expression.

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OsNAC45 is Involved in ABA Response and Salt Tolerance in Rice

Rice ◽

10.1186/s12284-020-00440-1 ◽

2020 ◽

Vol 13 (1) ◽

Author(s):

Xiang Zhang ◽

Yan Long ◽

Jingjing Huang ◽

Jixing Xia

Keyword(s):

Transcription Factors ◽

Salt Stress ◽

Salt Tolerance ◽

Stress Responses ◽

Crop Yields ◽

Plant Stress ◽

Root Cells ◽

Nac Transcription Factors ◽

Rice Plants ◽

Plant Stress Responses

Abstract Background Salt stress threatens crop yields all over the world. Many NAC transcription factors have been reported to be involved in different abiotic stress responses, but it remains unclear how loss of these transcription factors alters the transcriptomes of plants. Previous reports have demonstrated that overexpression of OsNAC45 enhances salt and drought tolerance in rice, and that OsNAC45 may regulate the expression of two specific genes, OsPM1 and OsLEA3–1. Results Here, we found that ABA repressed, and NaCl promoted, the expression of OsNAC45 in roots. Immunostaining showed that OsNAC45 was localized in all root cells and was mainly expressed in the stele. Loss of OsNAC45 decreased the sensitivity of rice plants to ABA and over-expressing this gene had the opposite effect, which demonstrated that OsNAC45 played an important role during ABA signal responses. Knockout of OsNAC45 also resulted in more ROS accumulation in roots and increased sensitivity of rice to salt stress. Transcriptome sequencing assay found that thousands of genes were differently expressed in OsNAC45-knockout plants. Most of the down-regulated genes participated in plant stress responses. Quantitative real time RT-PCR suggested that seven genes may be regulated by OsNAC45 including OsCYP89G1, OsDREB1F, OsEREBP2, OsERF104, OsPM1, OsSAMDC2, and OsSIK1. Conclusions These results indicate that OsNAC45 plays vital roles in ABA signal responses and salt tolerance in rice. Further characterization of this gene may help us understand ABA signal pathway and breed rice plants that are more tolerant to salt stress.

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Comprehensive Analysis of the Histone Deacetylase Gene Family in Chinese Cabbage (Brassica rapa): From Evolution and Expression Pattern to Functional Analysis of BraHDA3

Agriculture ◽

10.3390/agriculture11030244 ◽

2021 ◽

Vol 11 (3) ◽

pp. 244

Author(s):

Seung Hee Eom ◽

Tae Kyung Hyun

Keyword(s):

Functional Analysis ◽

Brassica Rapa ◽

Chinese Cabbage ◽

Stress Responses ◽

Histone Deacetylases ◽

Expression Patterns ◽

Evolutionary Relationship ◽

Gene Families ◽

Physiological Processes ◽

Lysine Residues

Histone deacetylases (HDACs) are known as erasers that remove acetyl groups from lysine residues in histones. Although plant HDACs play essential roles in physiological processes, including various stress responses, our knowledge concerning HDAC gene families and their evolutionary relationship remains limited. In Brassica rapa genome, we identified 20 HDAC genes, which are divided into three major groups: RPD3/HDA1, HD2, and SIR2 families. In addition, seven pairs of segmental duplicated paralogs and one pair of tandem duplicated paralogs were identified in the B. rapa HDAC (BraHDAC) family, indicating that segmental duplication is predominant for the expansion of the BraHDAC genes. The expression patterns of paralogous gene pairs suggest a divergence in the function of BraHDACs under various stress conditions. Furthermore, we suggested that BraHDA3 (homologous of Arabidopsis HDA14) encodes the functional HDAC enzyme, which can be inhibited by Class I/II HDAC inhibitor SAHA. As a first step toward understanding the epigenetic responses to environmental stresses in Chinese cabbage, our results provide a solid foundation for functional analysis of the BraHDAC family.

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Clade III cytokinin response factors share common roles in response to oxidative stress responses linked to cytokinin synthesis

Journal of Experimental Botany ◽

10.1093/jxb/erab076 ◽

2021 ◽

Vol 72 (8) ◽

pp. 3294-3306

Author(s):

Ariel M Hughes ◽

H Tucker Hallmark ◽

Lenka Plačková ◽

Ondrej Novák ◽

Aaron M Rashotte

Keyword(s):

Oxidative Stress ◽

Transcription Factors ◽

Stress Response ◽

Stress Responses ◽

Oxidative Stress Response ◽

Response Factors ◽

Ontology Term ◽

Regulated Expression ◽

Cytokinin Response ◽

Oxidative Stress Responses

Abstract Cytokinin response factors (CRFs) are transcription factors that are involved in cytokinin (CK) response, as well as being linked to abiotic stress tolerance. In particular, oxidative stress responses are activated by Clade III CRF members, such as AtCRF6. Here we explored the relationships between Clade III CRFs and oxidative stress. Transcriptomic responses to oxidative stress were determined in two Clade III transcription factors, Arabidopsis AtCRF5 and tomato SlCRF5. AtCRF5 was required for regulated expression of >240 genes that are involved in oxidative stress response. Similarly, SlCRF5 was involved in the regulated expression of nearly 420 oxidative stress response genes. Similarities in gene regulation by these Clade III members in response to oxidative stress were observed between Arabidopsis and tomato, as indicated by Gene Ontology term enrichment. CK levels were also changed in response to oxidative stress in both species. These changes were regulated by Clade III CRFs. Taken together, these findings suggest that Clade III CRFs play a role in oxidative stress response as well as having roles in CK signaling.

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Msn2- and Msn4-Like Transcription Factors Play No Obvious Roles in the Stress Responses of the Fungal Pathogen Candida albicans

Eukaryotic Cell ◽

10.1128/ec.3.5.1111-1123.2004 ◽

2004 ◽

Vol 3 (5) ◽

pp. 1111-1123 ◽

Cited By ~ 97

Author(s):

Susan Nicholls ◽

Melissa Straffon ◽

Brice Enjalbert ◽

André Nantel ◽

Susan Macaskill ◽

...

Keyword(s):

Candida Albicans ◽

Transcription Factors ◽

Stress Responses ◽

Ectopic Expression ◽

Heavy Metal Stress ◽

Luciferase Reporter ◽

Response Element ◽

Dna Binding Domains ◽

Binding Domains ◽

Adverse Environmental Conditions

ABSTRACT In Saccharomyces cerevisiae, the (C2H2)2 zinc finger transcription factors Msn2 and Msn4 play central roles in responses to a range of stresses by activating gene transcription via the stress response element (STRE; CCCCT). The pathogen Candida albicans displays stress responses that are thought to help it survive adverse environmental conditions encountered within its human host. However, these responses differ from those in S. cerevisiae, and hence we predicted that the roles of Msn2- and Msn4-like proteins might have been functionally reassigned in C. albicans. C. albicans has two such proteins: CaMsn4 and Mnl1 (for Msn2- and Msn4-like). CaMSN4, but not MNL1, weakly complemented the inability of an S. cerevisiae msn2 msn4 mutant to activate a STRE-lacZ reporter. Also, the disruption of CaMsn4 and Mnl1 had no discernible effect upon the resistance of C. albicans to heat, osmotic, ethanol, nutrient, oxidative, or heavy-metal stress or upon the stress-activated transcriptome in C. albicans. Furthermore, although Cap1-dependent activation of a Yap response element-luciferase reporter was observed, a STRE reporter was not activated in response to stresses in C. albicans. Ectopic expression of CaMsn4 or Mnl1 did not affect the cellular or molecular responses of C. albicans to stress. Under the conditions tested, the putative activation and DNA binding domains of CaMsn4 did not appear to be functional. These data suggest that CaMsn4 and Mnl1 do not contribute significantly to stress responses in C. albicans. The data are consistent with the idea that stress signaling in this fungus has diverged significantly from that in budding yeast.

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RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry

Journal of Experimental Medicine ◽

10.1084/jem.20120565 ◽

2012 ◽

Vol 209 (13) ◽

pp. 2409-2422 ◽

Cited By ~ 77

Author(s):

Heiyoun Jung ◽

Benjamin Hsiung ◽

Kathleen Pestal ◽

Emily Procyk ◽

David H. Raulet

Keyword(s):

Cell Cycle ◽

Transcription Factors ◽

Stress Responses ◽

Transcriptional Activation ◽

Posttranscriptional Regulation ◽

Cellular Proliferation ◽

Control Cell ◽

T Cell Subsets ◽

Cell Cycle Entry

The NKG2D stimulatory receptor expressed by natural killer cells and T cell subsets recognizes cell surface ligands that are induced on transformed and infected cells and facilitate immune rejection of tumor cells. We demonstrate that expression of retinoic acid early inducible gene 1 (RAE-1) family NKG2D ligands in cancer cell lines and proliferating normal cells is coupled directly to cell cycle regulation. Raet1 genes are directly transcriptionally activated by E2F family transcription factors, which play a central role in regulating cell cycle entry. Induction of RAE-1 occurred in primary cell cultures, embryonic brain cells in vivo, and cells in healing skin wounds and, accordingly, wound healing was delayed in mice lacking NKG2D. Transcriptional activation by E2Fs is likely coordinated with posttranscriptional regulation by other stress responses. These findings suggest that cellular proliferation, as occurs in cancer cells but also other pathological conditions, is a key signal tied to immune reactions mediated by NKG2D-bearing lymphocytes.

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