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Identification of drought, cadmium and root-lesion nematode infection stress-responsive transcription factors in ramie

  • Xia Zheng , Siyuan Zhu , Shouwei Tang and Touming Liu EMAIL logo
Published/Copyright: September 9, 2016
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Open Life Sciences
From the journal Open Life Sciences Volume 11 Issue 1

Abstract

Drought, cadmium (Cd) stress, and root lesion nematode (RLN) infection are three of the most important stresses affecting ramie growth and development; therefore, ramie breeding programs focus on their management more than on any other abiotic or biotic stresses. The fact that only a small number of stress-responsive transcription factors (TFs) have been identified so far is a major obstacle in the elucidation of mechanisms regulating the response to these three stresses in ramie. In this study, in order to uncover more stress-responsive TFs, a total of 179 nonredundant genes with full-length open reading frames from the MYB, AP2/ERF, bZIP, HD-ZIP, and COL families were obtained by searching for against the ramie transcriptome. Expression pattern analysis demonstrated that most of these genes showed relatively higher expression in the stem xylem and bast than in other tissues. Among these genes, 96 genes were found to be involved in responses to drought, Cd exposure, or RLN-infection. The expression of 54 of these genes was regulated by at least two stresses. These stress-responsive TFs probably have roles in the regulation of stress tolerance. The discovery of these stress-responsive TFs will be helpful for furthering our understanding of the mechanisms that regulate stress responses in ramie.

Keywords: Ramie; drought stress; cadmium stress; RLN infection; transcription factor; qRT-PCR

1 Introduction

Ramie (Boehmeria nivea L. Gaud), commonly known as China grass, is one of the most important natural fiber crops in Asia. Ramie fibers, stripped from the stem bast, possess many useful characteristics, such as smooth texture, extensive length, and excellent tensile strength. These characteristics have made ramie a widely cultivated crop in China, India, and other Southeast Asian and Pacific Rim countries.

Drought is a major environmental stress that affects the growth and development of ramie [1]. Ramie exhibits vigorous vegetative growth and can be harvested three times per year in China, and up to six times per year in well-watered agricultural environments in the Philippines. Therefore, in order to meet high metabolic requirements for vegetative growth of ramie, a sufficient supply of water is essential. When ramie suffers from water deficit, stem growth is severely inhibited, and fiber yield becomes significantly lower [2,3]. Additionally, infection by root-lesion nematodes (RLN) is a major biotic stress that influences vegetative growth of agricultural ramie. Pratylenchus coffeae is the major RLN species that infects ramie, and causes severe root damage, thus hindering absorption of water and nutrients from the soil. Ultimately, the result of the RLN infection is inhibition of growth and a significant decrease in fiber yield [4,5].

Recently, contamination of agricultural soils with cadmium (Cd) has become a major environmental problem in China [6]. Ramie can absorb and accumulate large amounts of Cd in its tissues [6–8]. Unlike food crops, which introduce Cd accumulated in the plant tissues into the food chain, the textile fiber crop ramie has no effect on animal and human health [7]. Hence, ramie has frequently been proposed as a potential phytoremediation crop for the restoration of Cd-contaminated farmlands [6–8]. Although ramie has a high tolerance to Cd stress, its growth is still greatly inhibited by high concentrations of Cd in the soil (more than 100 mg Cd per kg of dry soil). Morphological and physiological characteristics that are noticeably affected by Cd toxicity include plant height, stem diameter, bark thickness, chlorophyll content, and soluble protein content [6,8–10].

Improvement of tolerance to drought, Cd stress, and RLN infection is one of the most important goals in ramie breeding programs. Therefore, it is essential to determine the profile of the expression of stress-responsive genes in ramie and to elucidate the response mechanisms to these three stresses. The use of the Illumina sequencing technology for genome-wide transcriptome profiling of ramie has uncovered global expression signatures of the genes that respond to these three stresses [3,11,12]. Those stress-induced genes not only function to protect cells from stress through the production of important enzymes and metabolic molecules (i.e., functional proteins), but they also modulate signal transduction and gene expression during stress responses by encoding regulatory proteins. Transcription factors (TFs) are thought to be important regulatory proteins that modify stress responses in plants. However, based on genomewide transcriptomic profiling analyses, not more than 100 TFs were identified to be involved in modulating responses to drought, Cd stress, or RLN infection in ramie [3,11–13], which is far from sufficient to understand the network that regulates responses to these three stresses. In this study, in order to identify other TFs that may be involved in mechanisms of tolerance to drought, Cd stress, and RLN infection, the genes with full-length open reading frames (ORF) from five TF families (MYB, HD-ZIP, bZIP, AP2/ERF and COL) were mined in the ramie transcriptome [14,15]. Thereafter, changes in expression of these identified genes after drought, exposure to Cd, or RLN infection were systematically investigated by using qRT-PCR. Identification of these stress-responsive TFs will provide the basis for future clarification of their function in the regulation of stress tolerance. It will also be a useful gene resource that could facilitate improvements in stress tolerance in ramie breeding programs.

2 Materials and methods

2.1 Screening full-length ORF-containing genes from five TF families

Transcriptome of two ramie varieties, Qingyezhuma (QYZM) and Zhongzhu 1 (ZZ1) have been characterized using the Illumina sequencing technology [14, 15]. A total of 56,932 and 59,246 unigenes were assembled de novo from the QYZM and ZZ1 ramie varieties, respectively. Of these, 9,933 QYZM and 16,698 ZZ1 genes had full-length ORFs [15]. In order to find the MYB genes, the keyword “MYB” was used as a query to search for the annotations of these 26,631 genes with full-length ORFs. “Basic-leucine zipper” or “bZIP” were used as keywords to find the bZIP genes. ‘‘AP2,’’ “APETALA 2,” “Ethylene-responsive transcription factor,” “ERF,” “DREB,” or “Dehydration-responsive element-binding protein” were used as query keywords to search for the AP2/ERF genes. The keywords “Homeobox-leucine zipper” or “HD-ZIP” were used as queries to search for HD-ZIP genes, and “COL,” “CCT,” and “CONSTANS” were used to find the COL genes. The genes from the two varieties that belonged to the same families were aligned based on their nucleotide sequences using Clustal X [16]. The genes from the two different varieties that had an overlap of more than 200 bp were considered to be the same gene, and the ones with longer nucleotide sequences were selected. Additionally, genes that were found in only one variety were set aside. All non-redundant putative protein sequences from each family were manually checked for their conserved family domains.

2.2 Phylogenetic analysis of proteins from five TF families

Non-redundant putative sequences of proteins from five families were used in the phylogenetic analysis. Sixteen COL genes from other species have been characterized for their function [17], and they are listed in Table S1. These 16 COL proteins, together with the ramie COL proteins identified in this study, were used for the phylogenetic analysis of the evolutionary relationships between the COL genes of ramie and of other species. Multiple sequence alignments of the full-length protein sequences were constructed using the Clustal X (version 1.83) software program [16]. An unrooted phylogenetic tree was constructed with MEGA 4.0 using the neighbor-joining method. The bootstrap test was carried out with 1000 replicates [18].

2.3 Stress treatment, tissue sampling, and RNA extraction

Ramie seedlings were prepared by the cutting propagation method described by Yu et al. [19]. In April 2014, about 20 cm tall cuttage seedlings of Zhongzhu 1 were transplanted to round pots (diameter 20 cm and depth 13 cm) that were filled with 4 kg dry soil. One seedling was planted in each pot. These potted plants were grown under natural conditions in Changsha city, Hunan province, China (28°23’N, 112°93’E). After two months, the potted plants were split into two groups. One group included six potted plants, and three of these six plants were used for collection of tissue samples of the stem bast, xylem, shoots, leaves, and roots, separately (Figure S1), In Sept. 2014, the residual three plants in this group were used for sampling of the floral organ, including female and male flowers, when the potted ramie plants had flowered . These tissue samples were immediately frozen in liquid nitrogen and stored at –80 °C until analysis. Three samples of each tissue were stored separately as three independent biological replicates.

The other group, which included 12 potted plants, was used for stress experiments. The treatment methods were similar to those reported previously [20]. Three plants were exposed to drought stress by maintaining the relative water content of the soil below or equal to 35%. To examine the consequences of RLN infection, P. coffeae nematodes isolated from rotten ramie roots, and maintained on carrot discs were used as the inoculum to infect the ramie plants. Three plants were infected with P. coffeae nematodes by adding 1 mL of water containing 200 nematodes (mixture of juveniles and adults) to the soil near the roots of each ramie seedling. For the heavy metal treatment, three plants were treated with a solution of CdCl2•H2O, so that Cd concentration in every pot was 100 mg/kg dry soil. The drought stress treatment lasted for two days, whereas Cd and RLN stress treatment experiments were conducted for one week. After completion of the stress treatment experiments, all aerial and underground tissues of each plant were separately sampled. At the same time, the three potted plants grown under normal conditions were individually sampled as control replicates. All samples were immediately frozen in liquid nitrogen and stored at –80 °C until analysis.

Total RNA of each sample was extracted using an E.Z.N.A. Plant RNA Kit (OMEGA Bio-Tek, USA) according to the manufacturer’s protocol. The mRNA yield and quality were determined by spectrophotometry at 260 and 280 nm using the DU800 nucleic acid/protein analyzer (Beckman, USA). For each sample, first-strand cDNA molecules were reverse-transcribed from RNA treated with DNase I (Fermentas, Canada) by using M-MuLV Reverse Transcriptase (Fermentas) according to the manufacturer’s instructions.

2.4 qRT-PCR analysis and identification of stress-responsive genes

Three genes, namely, the cellulose synthase gene unigene21178, the actin gene, and the 18s ribosomal RNA gene, were used as candidate internal controls. The GeNorm program [21] was used to analyze stability of these three candidate internal controls. We found that unigene21178 was constantly expressed in six tissues, whereas the actin gene showed reliable and steady expression in both control and stressed ramie plants. Thus, the unigene21178 and the actin gene were used as the internal controls for the analysis of tissue specific expression and investigations of responses to different types of stress treatment, respectively. The primer sequences of all genes identified in this study, as well as those of the three candidate and internal control genes are listed in Table S2.

qRT-PCR was performed using an optical 96-well plate with an iQ5 multicolor real-time PCR system (Bio-RAD, USA). Each reaction contained 1.0 μL of the cDNA template from the reverse-transcribed reaction described above, 10 nM gene-specific primers, and 10 μL of the iTaqTM Universal SYBR Green supermix (Bio-RAD, USA), for a final volume of 20 μL. Thermal cycling by the iQ5 multicolor real-time PCR system (Bio-RAD, USA) was carried out as described by Liu et al. [20]. The values of the mean and standard error of nine Ct values (i.e., qRT-PCR was performed three times in each of the three biological replicates) were calculated for each sample. The relative expression levels were determined as previously described [22]. If gene expression levels under stress and in control conditions were found to be different with more than three-fold, the corresponding gene was considered to be stress-responsive.

3 Results

3.1 Identification of MYB, HD-ZIP, bZIP, AP2/ ERF, and COL genes with full-length ORFs

There are 56,932 and 59,246 unigenes in the QYZM and ZZ1 ramie varieties, respectively, which were previously assembled de novo via deep transcriptome sequencing [15]. Of these, 9,933 QYZM genes and 16,698 ZZ1 genes had full-length ORFs [15]. By mining these gene sets, we revealed 55 MYB, 24 AP2/ERF, 29 bZIP, 21 HD-ZIP, and 9 COL genes in the QYZM transcriptome. Furthermore, 54 MYB, 40 AP2/ERF, 14 bZIP, 24 HD-ZIP, and 6 COL genes were found in the ZZ1 transcriptome. In order to eliminate redundant genes, genes from the two ramie varieties that belonged to the same gene family were aligned based on their nucleotide sequences. Overall, 67, 43, 33, 25, and 9 non-redundant genes with full-length ORFs from the MYB, AP2/ERF, bZIP, HD-ZIP, and COL families were obtained, respectively (Tables 1, S3). These MYB, AP2/ERF, bZIP, HD-ZIP, and COL genes were designated BnMYB01 to BnMYB67, BnERF01 to BnERF43, BnbZIP01 to BnbZIP33, BnHDZIP01 to BnHDZIP25, and BniCOL1 to BniCOL11, respectively. Their sequences have been submitted to GeneBank under the accession numbers KP229557-KP229729 and KF928219-KF928224 (Tables 1, S3).

Table 1

Summary of genes identified from five TF families.

FamiliesNuber of GenesGene namesGenebank IDNumber of stress-responsive genes
DroughtCadmiumRLN-infection
MYB67BnMYB01-BnMYB67KP229557-KP229623211423
AP2/ERF43BnERF01-BnERF43KP229624-KP22966615118
bZIP33BnbZIP01-BnbZIP33KP229667-KP22969920158
HD-ZIP25BnHDZIP01-BnHDZIP67KP229700-KP2297241394
COL11BniCOL01-BniCOL11KF928219-KF928224, KP229725-KP229729312

3.2 Phylogenetic analysis of proteins

To elucidate the evolutionary relationships between the genes of each family, all protein sequences identified in this study were subjected to phylogenetic analysis. The results are shown in Figure 1. The MYB, AP2/ERF, bZIP, and HD-ZIP proteins could be distinctly classified into 7, 4, 4, and 4 subfamilies, respectively, except for a few proteins that were not assigned to any subfamily. In addition, we carried out a phylogenetic analysis of 11 ramie COL proteins and 16 COL proteins with known functions in other species, revealing that these 27 COL proteins could be classified into 4 groups with10 of the 11 ramie COL proteins assigned to two distinct groups (Figure 1).

Figure 1 Phylogenetic tree of all proteins in each family. For the COL family, 16 COL proteins with known functions in other species [19] and 11 ramie COL members were phylogenetically analyzed together. The unrooted tree was generated using the MEGA 4 program and the neighbor-joining method. The bootstrap test was carried out using 1000 replications. The TFs presented in blue font are stress-responsive proteins.
Figure 1

Phylogenetic tree of all proteins in each family. For the COL family, 16 COL proteins with known functions in other species [19] and 11 ramie COL members were phylogenetically analyzed together. The unrooted tree was generated using the MEGA 4 program and the neighbor-joining method. The bootstrap test was carried out using 1000 replications. The TFs presented in blue font are stress-responsive proteins.

3.3 Analysis of expression of identified genes in six tissues

In order to characterize the expression patterns of the 179 genes identified in different organs, the relative expression levels of these genes were analyzed in six tissues (leaf, stem bast, stem xylem, shoot, root, and flower). We found that, among the 67 MYB genes, there were 34, 22, and 33 genes with highest expression in the shoot, stem xylem, and stem bast, respectively; whereas only 4, 5, and 14 MYB genes were most highly expressed in the flower, root, and leaf tissues, respectively (Figure 2; Table S3). In addition, 28 AP2/ERF, 26 bZIP, 8 HD-ZIP, and 6 COL genes were more highly expressed in the stem xylem than in other tissues. Furthermore, 14 AP2/ERF, 10 bZIP, 15 HD-ZIP, and 2 COL genes were more highly expressed in the stem bast than in other tissues (Figure 2; Table S3). Only a few genes from the AP2/ERF, bZIP, HD-ZIP, and COL families exhibited greater transcript abundance in the flower, root, shoot, or leaf tissues than in the stem xylem and bast (Figure 2; Table S3).

Figure 2 Histograms which showed the number of genes with relatively high expression levels in each tissue, for each family. The y axis indicates six tissues investigated, and the number next to each histogram bar represents the number of genes with relatively high expression levels in the corresponding tissue in the respective family.
Figure 2

Histograms which showed the number of genes with relatively high expression levels in each tissue, for each family. The y axis indicates six tissues investigated, and the number next to each histogram bar represents the number of genes with relatively high expression levels in the corresponding tissue in the respective family.

3.4 Gene expression response to three different kinds of stress

Changes in expression of the 179 genes from five TF families to drought, Cd stress, and RLN infection were investigated, and genes with more than a three-fold expression change under stress were considered to be stress-responsive. The results indicated that there were 72 drought stress-responsive genes (55 and 17 genes with up- and down-regulated expression, respectively) and 50 Cd stress-responsive genes (31 and 19 genes with up-and down-regulated expression, respectively) (Tables 1, S3; Figure 3A). In addition, the expression levels of 45 genes were found to be affected by the RLN infection; the expression of 22 and 23 genes was up- and down-regulated, respectively (Tables 1, S3; Figure 3A). Expression levels of the majority of genes from the AP2/ERF and bZIP families were found to be up-regulated under the three stress conditions. In contrast, expression of most genes that belonged to the MYB and HD-ZIP families was down-regulated by stress treatments (Figure 3A; Table S3).

Figure 3 Quantitative data on genes responding to different kinds of stress. (A) The number of genes that changed their expression in response to drought, Cd stress, or RLN infection. Histogram bars on and under the x axis indicate the number of up and down-regulated genes, respectively. (B) The number of stress-responsive genes in each family. The red, blue, and purple circles represent the number of genes responding to drought, Cd stress, and RLN infection, respectively. The number written in the overlapping region of two or three circles indicates the number of genes that respond to two or three stresses.
Figure 3

Quantitative data on genes responding to different kinds of stress. (A) The number of genes that changed their expression in response to drought, Cd stress, or RLN infection. Histogram bars on and under the x axis indicate the number of up and down-regulated genes, respectively. (B) The number of stress-responsive genes in each family. The red, blue, and purple circles represent the number of genes responding to drought, Cd stress, and RLN infection, respectively. The number written in the overlapping region of two or three circles indicates the number of genes that respond to two or three stresses.

Of the 33 stress-responsive MYB genes, expression of 19 genes was altered by several types of stress (Figure 3B; Table S3). There were 21 and 25 stress-responsive AP2/ERF and bZIP genes identified, respectively, of which 9 AP2/ERF and 14 bZIP genes were sensitive to at least two stress conditions (Figure 3B; Table S3). In addition, expression of 14 HD-ZIP and 3 COL genes was regulated by stress, and expression levels of 10 HD-ZIP and 2 COL genes were influenced by multiple types of stress (Figure 3B; Table S3).

4 Discussion

4.1 Comparison of the stress-responsive TFs between this study and previous studies

Recently, expanding transcriptome datasets have uncovered a global picture of plant genes responsive to various abiotic and biotic stresses. Hundreds of transcription factors (TFs) have been found to modulate tolerance to various abiotic and biotic stresses [23–26]. Most of these TFs, which belong to several large TF families, such as AP2/ERF, bZIP, COL, MYB, HD-ZIP, and NAC, regulate expression of downstream target genes that are involved in plant tolerance to various stresses [27–29].

Drought, Cd stress, and RLN infection are three of the most important stresses affecting growth and development of ramie. In breeding programs, improving tolerance to these three stresses is given more attention than to defense against other abiotic and biotic stresses. Sixty-nine stress-responsive TFs, including five NAC TFs, have been identified via genome-wide expression profiling using the Illumina sequencing method [3,11,12]. In our previous study, by qRT-PCR analysis, we determined that out of 32 full-length NAC genes identified in ramie, 19 NAC genes had their expression altered by one or more of these three stress conditions [20]. It seems that qRT-PCR analysis has a higher sensitivity in detecting stress-responsive genes than the Illumina sequencing method. In addition, only 19 stress-responsive TFs in MYB, AP2/ERF, bZIP, HD-ZIP, and COL TFs families have been identified by the Illumina sequencing method (Table S4) [3,11,12]. Therefore, in order to reveal additional, previously undiscovered stressresponsive TFs from these five TF families, we examined changes in gene expression caused by drought, Cd stress and RLN-infection by using qRT-PCR analysis. A total of 96 stress-responsive genes in these five families have been identified. Thus, our study extended the number of stressresponsive TFs from the five TFs families from 19 to 96. Out of the 19 stress-responsive genes identified by Illumina sequencing in previous studies, we confirmed, using qRT-PCR, 13 genes that change their expression in stress conditions (Table S4). Expression of 4 out of those 19 genes did not differ between samples from stress-treated and control ramie according to our qRT-PCR analysis, which suggested that differential expression of these four genes in the Illumina study could be a false positive result (Table S4). The remaining two genes from the Illumina study have not been investigated here, because they do not have full-length ORFs. Identification of these 96 stress-responsive TFs will provide a basis for a further clarification of their potential functions in the regulation of stress tolerance.

4.2 Stress-responsive TFs possibly regulate tolerance in ramie

Many members of MYB, AP2/ERF, bZIP, and HD-ZIP families not only play important roles in the regulation of plant tolerance to abiotic stresses, but also function as regulators of responses to biotic stress, particularly with respect to activation of anti-pathogen defenses [30–39]. In rice, transgenic technology approaches indicated that at least five bZIP genes, nine AP2/ERF genes, and one MYB genes regulated tolerance to drought [40]. In Arabidopsis, at least three bZIP genes, six AP2/ERF genes, four HD-ZIP genes and six MYB genes were found to be important regulators of tolerance to drought or other osmotic stresses [30]. Moreover, recent studies demonstrated that several COL genes are involved in responses to drought or other osmotic stresses [41]. Overexpression of the rice gene Ghd7 and Arabidopsis AtCOL4 revealed that these genes play important roles in regulating responses to drought and other osmotic stresses [42,43]. These TFs were part of the drought-stress regulatory network in corresponding species. In relation to the Cd-induced stress, although differential expression analysis identified many stress-responsive TFs in rice [44] and Arabidopsis [45], there are still too few clues regarding their precise functions in modulating tolerance to Cd. Previous reports confirmed that Cd stress-responsive TFs are probably associated with the same signal transduction pathway that is activated by other abiotic stresses, such as cold, dehydration, salicylic acid, or H2O2 [46].

Recently, it was found that overexpression of SNAC1, a NAC gene known to regulate tolerance to drought in rice, remarkably improved tolerance to drought and excessive salinity in ramie [47]. This finding suggested that ramie likely possesses a regulatory stress tolerance network similar to that of rice. Moreover, in model plant rice and Arabidopsis, the regulatory network of stress tolerance has been characterized, and was found to comprise multiple MYB, AP2/ERF, bZIP, and HD-ZIP genes [30, 40]. In the present study, changes in expression of a total of 96 genes from MYB, AP2/ERF, bZIP, COL, and HD-ZIP TF families were observed as a result of drought, Cd stress, or RLN-infection. Probably, in similarity to findings concerning the roles of TFs from MYB, AP2/ERF, bZIP, COL, and HD-ZIP families in model plants [30,40], the 96 stressresponsive TFs identified in our study potentially have a role in regulating stress tolerance in ramie.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31571725), the Agricultural Science and Technology Innovation Program (ASTIP) and National Modern Agroindustry Technology Research System (nycytx-19-E16).

  1. Conflict of interest: The authors declare that they have no conflict of interest.

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Received: 2016-2-4
Accepted: 2016-6-23
Published Online: 2016-9-9
Published in Print: 2016-1-1

© 2016 Xia Zheng et al., published by De Gruyter Open

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

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https://doi.org/10.1515/biol-2016-0025
Keywords for this article
Ramie; drought stress; cadmium stress; RLN infection; transcription factor; qRT-PCR
Creative Commons
BY-NC-ND 3.0

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  2. Purification of polyclonal IgG specific for Camelid’s antibodies and their recombinant nanobodies
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  4. Antioxidative defense mechanism of the ruderal Verbascum olympicum Boiss. against copper (Cu)-induced stress
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  110. Effect of miRNAs in lung cancer suppression and oncogenesis
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  115. Special Issue on CleanWAS 2015
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  118. Genetic diversity and population structure of ginseng in China based on RAPD analysis
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