Genome Wide Analysis and Characterization of Heat Shock Transcription Factors (Hsfs) in French Bean (Phaseolus Vulgaris L.)

doi:10.21203/rs.3.rs-36054/v1

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Genome Wide Analysis and Characterization of Heat Shock Transcription Factors (Hsfs) in French Bean (Phaseolus Vulgaris L.)

https://doi.org/10.21203/rs.3.rs-36054/v1

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Background: Heat shock transcription factors (HSFs) play an important role as transcriptional regulatory proteins against heat stress by controlling the expression of heat responsive genes. French bean is a highly thermosensitive crop and therefore, its genome sequence information segregated, characterized here in terms of heat shock transcription factors alongwith its evolutionary significance.

Results: In this study, a total comprehensive set of 29 non-redundant full length HSF genes were identified and characterized from Phaseolus vulgaris L. (PvHSF) genome sequence. Detailed gene information such as chromosomal localization, domain position, motif organization and exon- intron identification were analyzed. All the 29 PvHSF genes were mapped on 8 out of 11 chromosomes indicating the gene duplication occurred in french bean genome. Motif analysis and exon- intron structure found to be conserved in each group which showed conserved structure of PvHSFs and heat induced response is highly influenced by the cytoplasmic proteins. Based on structural features and phylogenetic relationship, the HSF genes were grouped into three classes i.e. A to C and 14 groups. Presence of only one pair of paralog sequence suggests that it may be derived from the duplication event during evolution. Comparative genomics study indicated the influence of whole genome duplication and purifying selection on french bean genome during evolution. In silico expression analysis indicated active role of classs A and B family during abiotic stress condition and higher expression in floral organs.

Conclusion: A comprehensive analysis of Heat shock transcription factors resulted 29 non-redundant full length PvHSF genes, which were characterized for their occurrence in genome and functional importance through In silico approach.

Plant Molecular Biology and Genetics

Plant Physiology and Morphology

PvHSF

heat stress

french bean

Phaseolus vulgaris

evolution

Plants are the ancient organisms which have been confronted to various biotic and abiotic stress during the course of evolution through regulatory network of inherent adaptation measures. As sessile organisms, plants cannot avoid different biotic and abiotic stresses by changing their positions [1, 2]. Abiotic stress conditions such as transitory or constantly increasing temperature, drought, salinity, high light intensity, exposure to Ozone (Oȝ), chilling, freezing, exposure of the cell to toxins (ethanol, arsenic, trace metals, UV light) have considerable impact in the plant yield as it can reduce more than 50% productivity in many species. Heat stress is a major stress which causes the protein denaturation affecting the cytoskeleton arrangement of the cell and induces disruption in the metabolism, photosynthesis activity and cell membrane structure. Stressful environmental condition causes morpho-anatomical, physiochemical and biochemical changes at cellular level, which may affect the plant biomass production and economic yield in many areas worldwide. Therefore, major objective of agronomic research is to increase crop productivity under biotic and abiotic stresses.

In recent years, it have been proved that all living organisms possesses a common heat shock response mechanism which initiates the synthesis of “Heat shock proteins” known as “Stress induced proteins” required for development of short term stress resistance [3, 4]. Among all 64 identified transcription factor groups in plants, Heat shock transcription factor family is ubiquitous and responsible for the expression of the heat shock proteins. Stress induced gene expression leads to the rapid accumulation of heat shock proteins which belong to 11 conserved multi-protein families. As the major HSPs are highly homologous among eukaryotes, the evolutionary conservation of the heat shock response is evidence which justifies that the production of HSPs is a fundamental and imperative process [5].

Characteristic feature of transcription factors is that they contain one or more DNA binding domain which binds to the promoter region for gene expression [6]. In general, HSF proteins have a core structure consisting a N- terminal DNA binding domain made up of a four-stranded antiparallel β-sheet and three helical bundle. It is characterized by a central helix-turn-helix (HTH) motif which recognizes and binds to the conserved cis acting elements known as “Heat Shock Element” (HSEs;5-AGAAnnTTCT-3). An adjacent domain commonly known as oligomerization domain with a heptad hydrophobic repeat (HR-A/B) required for the trimerization of HSF is connected to the DBD region by a linker group of amino acids. Arginine(R)& Lysine(K) rich NLS region and Leucine (L) rich NES regions are responsible for the dynamic distribution of HSF between the nucleus and cytoplasm [7, 8]. It has been seen that in most cases class A and C HSFs are having monopartite and bipartite NLSs (nuclear localization signals) adjacent to the oligomerization domain. AHA (Aromatic large hydrophobic amino acid residues) motif or the activation domain is the least defined part of HSF which consists of activators and repressor elements. It is a characteristic region of class A HSFs as class B and C lacks AHA motif. It is required for the transcription of HSPs, by binding to some basic transcription protein complexes. [9, 10].

In plants, ubiquity of heat shock proteins was first observed in Glycine max and Tobacco, using cell culture technique which revealed synthesis of certain proteins under heat condition. To our knowledge, HSFs have been investigated in many plats including Lycopersicon peruviannum (tomato), Arabidopsis thaliana, Zea mays (maize), Glycine max (soybean), Medicago truncatula (barrel clover), Lotus japonicus, Triticum aestivum (wheat), Oryza sative (rice), Vigna radiata (mung bean), Populus trichocarpa (black cottonwood). Here, well described 21 Arabidopsis HSF gene are used as seed sequence in order to identify and characterize the pool of HSF genes present in Phaseolus vulgaris (French bean) genome.

Material and methods:

Identification of HSFs:

Amino acid sequences corresponding to the 15 AtHSFs (A. thaliana) genes were retrieved from TAIR (The Arabidopsis Information Resource; http://www.Arabidopsis.org/. These protein sequences were used as query against database of Phytozome (http://www.phytozome.net)in standalone blast search with e values 0.001. Self-BLAST performed for sequences to remove redundancy. All the protein sequences thus obtained were confirmed with HMMER3.0 (http://hmmer.org/) on the basis of the HMM profile. Results from BLAST and HMMER hits were matched and parsed manually.

Characterization of HSF genes, chromosomal localization and protein domains:

To predict the physico-chemical properties, ProtParam tool (www.expacy.org/tools/protparam.html) was used. This tool is useful for computing the molecular weight, theoretical pI, amino acid composition, atomic composition, extinction coefficient, estimated half-life, instability index, aliphatic index, and grand average of hydropathicity (GRAVY). The subcellular localization predicted by CELLO for eukaryotic sequences. PROSITE was used for documentation and information about the protein domains, functions, families as well as patterns and profiles (http://prosite.expacy.org/). MacDraw, a Raster based and vector graphic drawing application used for drawing chromosomal map. Gene structure display server (GSDS) was used for illustrating the gene structure.

Conserved domains, motif prediction and promoter region identification:

PSort and NetNES results used for predicting the NLS (Nuclear Localization Signal) and NES (Nuclear Export signal) regions, respectively. Using the amino acid sequences as query, the servers predicted possible regions in the sequence. DBD region and coiled coil regions were identified from the COIL server and HMMER server results. Using MEME suite server, the conserved motifs were predicted in 29 putative identified proteins. Minimum width and maximum width for motifs were decided 10 and 50 respectively in the advance option menu. The highly conserved motifs identified in species using MAST algorithms (http://meme.nbcr.net/).

Class A HSF genes in GTF/GFF3 format were analyzed by PLANTCARE database for finding the cis-acting elements. PLACE database was used for understanding the functionality of the promoter regions.

Multiple sequence alignment and phylogeny analysis:

Phylogeny analysis has always been an important factor for understanding the evolutionary relationship among species. Total 100 HSFs from A. thaliana (21), G. max (26), V. radiate (24) and P. vulgaris (29) were aligned using Clustal Omega program. The alignment file was used for constructing the phylogeny tree using Neighbor Joining algorithm with 1000 bootstrap replications and wrapped in MEGA 7.

Comparative Analysis:

Ortholog and paralog genes are two different types of homologous genes derived from the ancestral DNA by speciation and duplication events, respectively. Paralog sequences were identified by performing similarity search among the PvHSF proteins. OrthoVenn2 server was used for prediction of the ortholog genes present in other species. By performing BLAST program among the HSF proteins retrieved from different species, ortholog sequences were found in Vigna radiata, Glycine max, Populous trichocarpa, Medicago truncatula and Arabidopsis thaliana. CoGe database was used for analyzing and visualizing the synteny between Phaseolus vulgaris and Arabidopsis thaliana.

Expression Analysis:

For expression analysis of identified PvHSFs, GEO dataset (Accession: GSE 123381) were retrieved from NCBI. The EST sequence information were retrieved from Phytozome database and used for tissue specific expression analysis retrieved. Heat map visualization and further editing was carried out by using the “gplot” package of R studio.

Identification and characterization of PvHSFs:

Two strategies were used to search for members of HSFs in French bean. Hidden Markov Model (HMM) and Standalone BLAST+ (version 2.2.23) software package. Sixty-five HSF loci were reported from Standalone BLAST against database Phytozome based on e value and identity percentage and score with significant alignments. Further with threshold e value and removal of incomplete, unanchored and redundant sequences, 29 PvHSF non-redundant candidate genes were identified which were similar with results of HMM search and characterized for biochemical properties and subcellular localization (Table 1, S1. PV_sequence). All the 29 PvHSF genes were mapped onto 11 Phaseolus vulgaris chromosomes (Figure 1). PvHSF genes were widely distributed in every chromosome except chromosome V, X and XI. Whereas, Chromosome I and II contains maximum number of genes i.e. 6 (20.68%) and 7 (24.13%), respectively. Five HSFs were detected on chromosome VII and four on chromosome III apart from single pair on Chromosome IV, VI and IX and chromosome VIII occupied only one HSF gene.

The key domain characterized by PROSITE results, which provided information about HSF_DOMAIN. The DBD domain located towards the N-terminal of sequence followed by oligomerization domain. PSort resulted absence of NLS region in class B including PvHSFA8 and PvHSFA3. However, NES region is present in all the classes except few members. Through comparison analysis, conserved AHA motif was observed towards the C-terminal only in Class A HSFs. Using COILS and HMMER results, identified the coiled coil region, a characteristic of HR-A/B region (Table 2). The MEME suite server predicted conserved motifs of PvHSFs proteins. Thirty corresponding consensus motifs were predicted (Fig. 2). The members of class A contained the most conserved motifs with largest number 11 detected in PvHSFA1A and PvHSFA1D. Class B members possessed 3-7 motifs while 4 motifs aligned in member of class C family i.e. PvHSFC1. Motifs 1, 2 and 4 represent the HSF DBD domains found in all 29 PvHSFs. Motif 3 represents the HR-A/B domain from the class A and C HSFs. All class B HSF proteins exhibited the coiled-coil region of HR-A/B domain by motif 5. Motif 6 represents HR-A/B domain from class A HSFs. Motif 7 conserved for NLS domains in class A while motif 8 conserved for NLS of B class families. Furthermore, motifs 10, 11, 14, 16, 17, 18, 23, 26, 28 and 30 represented NES domains with (L) leucine rich. AHA motifs identified by 9, 15, 16, 20, 21, 22, 24 and 29 with W (tryptophan) rich domain.

Gene structure and phylogeny analysis:

In this study, the structure of HSF gene with one intron found to be mostly conserved throughout subfamilies among 72.41% of PvHSF members (Fig. 3). However, length and location of intron varies among the HSFs. Noticeably, two introns were observed among 24.13% of HSFs genes of which all belongs to class A subfamilies (PvHSFA1B, PvHSFA2A, PvHSFA4C, PvHSFA7A, PvHSFA8, PvHSFA9A) except PvHSFB2C of class B. PvHSFA2B comprised of 3 introns with comparative smaller length.

The phylogenetic tree was constructed using MEGA 7 software with Neighbor-Joining method using multiple sequence alignment of 2 leguminosae members (Glycine max; GmHSFs and Vigna radiata; VrHSFs), 21 AtHSF and 29 PvHSF genes which categorized the 29 PvHSFs into 3 classes (A, B and C) and 14 groups (Fig. 4). Class A was the largest and contained 17 PvHSF which were again divided into 9 groups. Class B contained 11 members and Class C was the smallest consisting only one gene.

Regulatory cis acting elements

Sixty-four different promoter regions responsible for various expression identified among members (Table S2). The PvHSFA5.2 contented maximum number of promoter regions while PvHSFA4C identified for least. CAAT-box and MYC promoter region is present in all the class A HSFs gene while MYB promoter region is present in all the members except PvHSFA4 sub-group. ABRE (ABA responsive element) promoter region carried by all members except PvHSFA8 and A6 group. DRE region was only seen in PvHSFA4A and LTRE was observed in PvHSFA5.2 and PvHSFA9A. P-box, W- box, box S, G-box and I-box were observed in members of class A. Light responsive element, 3-af1 binding site was only observed in PvHSFA1B.

Comparative genomics

For synteny analysis, 11 HSF genes from 4 groups (A1, A2, A6, B2) were compared with their orthologs sequences present in Arabidopsis Thaliana. The synteny analysis (Fig. 6) revealed that PvHSFA2B, PvHSFA6A, PvHSFB2D are in synteny with their orthologs though microsynteny can be observed in maximum sequences. However, perfect synteny was observed in PvHSFB2D. For PvHSFA2A and A6B, the synteny was observed in between 100kb-110kb and 85kb-185kb, respectively. Least synteny was observed in PvHSFA1B/E, in which the regions from AtHSFA1E (70kb-130kb) distributed over 110 kb region (20kb-190kb). In PvHSFB2C, the widely distributed genes present in AtHSFB2B were conserved in 85kb to 100kb. From the comparative analysis, we found 22 orthologous clusters between HSFs of six plant spp. (Fig. 7). Only one pair of paralog sequences were found in french bean HSF family.

In silico expression analysis

The expression data showed 19 HSFs out of 29 PvHSF genes were upregulated under drought stress and highest expression of PvHSFB2A, indicating its master role under abiotic stress (Fig. 8a). The ubiquitous expression of PvHSFB2A throughout plant organs from ESTs dataset again supporting its key importance in gene regulatory network of french bean (Fig. 8b). Additionally, the relative expression of PvHSFA6B and PvHSFB2D were identified for having no or least expression in plant tissues.

Identification and characterization of HSF genes in French bean:

The HSF genes are ubiquitous and their numbers varies in organisms. However, number of HSFs in plants outnumbers other organisms. Although from different studies in plants, oftenly it counts from 16 to 82 (16; strawberry and 82; wheat; S3). Cytoplasmic occurrence of PvHSFs are similar to other HSFs like GmHSFs, LpHSFs [9, 11]. The 473 Mb of 587 Mb french bean genome has been sequenced and assembled [12]. This crop is absolutely diploid (2n= 2x=11), much smaller than soybean genome (1115 Mb) and significantly higher than arabidopsis (125 Mb). Subsequently, the number of protein coding genes significantly varies among arabidopsis (25kb), soybean (46.43kb) and french bean (31.64 kb). In above mentioned species, number of HSFs lying very close from 21 to 29 (21; arabidopsis, 26; soybean and 29; french bean) likely to cereal crop rice 25 (genome size: 389 Mb). Howsoever, 29 PvHSFs reported in this study is adjacent to other previous reported leguminoseae members i.e. 24 HSFs in Vigna radiata [3], 20 HSFs in Populous trichofera and 16 HSFs in Medicago truncatula [13]. These results indicate that difference in copies of HSFs among these plant species is independent of genome size or protein coding genes and conserved in plant species of family with moderate evolutionary events like whole genome duplication (WGD) followed by gene loss and purifying selection [14, 15]. Considering the total chromosome number, it can be observed that french bean has moderate number of HSF members being a member of legume family.

Gene features such as exon-intron distribution, gene length and GC content have acute impacts during evolutionary events like WGD. Various studies also indicated that introns are responsible not only for gene expression but also for gene evolution [16]. Similar to this, only one intron gene feature also reported from mung bean[3] and most of the HSF members of rosaceae family [17]. However, number of introns ranged from zero to two in Brassica oleracca [18], and zero to five in Brassica napus [19]. Though, at least one member of class C in Brassica napus and Brassica oleracca, lacks intron. These results indicating that during expansion and divergence of leguminosae HSFs, intron losses escaped and consequently presence of at least one intron and absence of intron lacking are characteristics of leguminoseae HSF gene family.

Invariably, all the plant HSFs have 3 classes in HSF family. Observing the phylogeny tree, french bean has comparatively higher number of members in each class of family except class C. For instance, 17 PvHSFs with respect to 13 VrHSFs while GmHSFs consists 19 members in this class. In other legumes, like Populus and Medicago consisted 15 and 10 members in Class A, respectively [9, 11]. However, 11 members of class B PvHSFs is quite conserved among family which ranged from 6-12 in above discussed legume species. Complete conservation of class C PvHSFs with only one gene is observed likely to Arabidopsis and legumes. This report is presenting the considerable evidence of tightly conserved Class C and moderate conservation of Class B members, however evolutionary events most frequently observed among Class A members. The phylogeny tree and distance matrix indicated that PvHSFs gene family more closely related to the VrHSFs with respect to GmHSFs.

Considering the importance of class A HSF subfamilies with conserved features which were observed to play important role during heat stress and therefore here PvHSFs members from Class A only analyzed through PLANTCARE database for understanding the cis-acting elements (Fig. 5). CAAT-box and MYC were found to be dominant elements present in all members of class A along with an unknown promoter region. MYB, STRE, LTRE, ABRE, DRE, MYC were some abiotic stress cis acting elements, found in class A PvHSFs. The above mentioned regions were reported to be important for heat shock response in plants. For instance, STRE was the first discovered cis acting element to be responsive to stress and provides binding site for HSFA1A in Arabidopsis Thaliana and deletion of STRE (Stress Responsive Elements) highly affects the promoter activity under stress condition. [20, 21]. In mung bean, all the genes were reported for having multiple DREs (Drought Responsive Elements) and ABREs. PvHSFA4A contained DRE1 responsible for dehydration response. DRE combining with DRE binding proteins (DREB 2A) involved in transcriptional regulation of stress in plants such as drought, salt and low temperature responses [22, 23]. LTR was observed in PvHSFA5.2 and PvHSFA9A which illustrates the low temperature response provided under stress condition [24]. Absence of LTRE in maximum members suggests lower response to low temperature in comparison to other plants. HSFa1a was reported before to be the master regulator for thermotolerance in tomato [25]. In Arabidopsis, it was reported that HSFA1a/b are responsible for the induction of class B genes under heat stress condition. [26, 27]. ABA responsive elements are also responsive to ABA and GA responses, via combination with ABRE binding proteins. In PvHSFA1A many ABA responsive elements like MYC and MYB were observed. Besides this, W box and box S, observed among several members responsible for wound responsive elements. Therefore, cis-element analysis of identified PvHSF members presents evidence of these genes for differential gene regulation during abiotic stress mostly thermotolerance and involvement in other regulatory functions like light responsive, wound responsive etc.

Synteny analysis of HSFs was performed between Phaseolus and Arabidopsis for the four different HSFs groups namely A1, A2, A6, and B2. These four HSFs groups showed highly conserved induced expression during heat stress in multiple crops such as rice, wheat, chickpea etc [1, 6, 14, 27]. Further, HSFA1a and HSFA2 was characterized as master regulator of basal and acquired thermotolerance, respectively in Arabidopsis, rice, tomato and other members of class A (A2 and A6) along with B2 functions as synergistic co activator. Therefore, considering their importance during heat stress response [9], a detailed analysis was conducted only for the members of these four HSFs groups (HSFA1, A2, A6 and B2) in our analysis. The synteny analysis (Fig.7) revealed that Arabidopsis HSFs and its orthologs in Phaseolus (PvHSFA2B, PvHSFA6A, PvHSFB2D) were in synteny and showed high degree of sequence conservation.

Specifically, perfect synteny was observed between Arabidopsis B2D and PvHSFB2D. However, PvHSFA2A and A6B showed synteny for the distance of 100kb-110kb and 85kb-185kb, respectively between Arabidopsis and Phaseolus. Besides, least synteny was observed for the HSFs namely PvHSFA1B/E, in which the regions from AtHSFA1E (70kb-130kb) was distributed over 110 kb region (20kb-190kb). Further, PvHSFB2C, the widely distributed genes present in AtHSFB2B were conserved in 85kb to 100kb. These findings in Phaseolus suggested that, during the course of evolution PvHSFA2B, PvHSFA6A and PvHSFB2D had conserved their gene structure in comparison with Arabidopsis indicating that the diversification might have took place due to speciation or duplication event. However, PvHSFB2C showed highly conserved synteny with 15 kn region. Additionaly, maximum members of Phaseolus HSFs showed microsynteny which can be correlated to the whole-genome duplication, gene loss or mutation [18, 20, 28].

Expressions of PvHSF genes under abiotic stress (drought) condition and tissue specific expression were illustrated with the objective of validation of putatively identified genes. The digital expression data (RPKM) from GEO datasets were retrieved and expressed in heatmap (Fig. 8a). This analysis shows that both class A and B family is directly involved in signaling pathways during abiotic stress. Also it may be inferred from this dataset that B4 group (a, b, c and d) of class B and A1 group (b and d), A3, A5.1 and A8 of class A alongwith PvHSFC1were upregulated during drought stress with wide variation. Likely to this class A and B family members played key role during heat stress driven experiments for instance, LpHSFA1 was reported to be the master regulator for thermotolerance in tomato [25]. Also two soybean HSFs from class A2 (GmHSF12, GmHSF 28) and 3 from class B (GmHSF 34, GmHSF 35 and GmHSF 47) were upregulated during stress condition [11]. Therefore, class A and B family members activation in signaling pathway during abiotic stress is established for PvHSF genes also. Ubiquitous expression of PvHSFB2A in all plant organs and highest even downregulated expression during abiotic stress stipulated its prime importance among all identified PvHSFs (Fig. 8b). However PvHSFB2D, B4C and D, PvHSFA6A and B had no expression in 1 to 4 organelles which is likely to PbHSFA6C of Chinese white pear where nil expression observed during its four developmental stages [17]. In french bean, PvHSFC1 has showed considerable expression in many samples and slight upreguation during drought stress showed its functional importance, but information is still incomplete.

In this study, a comprehensive set of 29 full length Heat shock factor genes (PvHSFs) were identified and characterized in Phaseolus vulgaris with additional gene information such as chromosomal localization and exon intron identification. All the genes were mapped on 8 out of 11 chromosomes indicating the gene duplication occurred in french bean genome. Motif analysis and exon intron structure found to be sustained in each group which concludes that structure of HSF family is conserved in french bean. It can be inferred that, heat shock response is highly influenced by the cytoplasmic proteins in french bean. According to the structural characteristics of the proteins and phylogeny analysis, the HSF genes were grouped into three classes (A, B and C) and 14 groups. Presence of only one pair of paralog sequence suggests that it may be derived from the duplication event during evolution. From the synteny analysis, it could be referred that whole genome duplication and purifying selection have highly influenced the french bean genome. Expression analysis validated class A and B HSFs involvement during abiotic stress and key importance of PvHSFB2A due to their comparative higher occurrence under abiotic stress and ubiquitous presence in floral organs. This comprehensive analysis establishes better understanding of PvHSF genes which will facilitate further functional characterization in french bean.

Contributors: The research topic was conceived and manuscript preparation including analysis was carried out by B. Mallick and Meenu Kumari, result interpretation was contributed by SK Pradhan and Parmeswaram C., editing and software scripts were supported by P Naresh and G C Acharya. All authors approved this manuscript.

Compliance with ethical standards: This article does not contain any studies with human participants or animals performed by any of the authors.

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

Funding Source: Not applicable.

Acknowledgement: Authors acknowledge Director, ICAR- IIHR and CHES, Bhubaneswar for providing basic facilities.

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Genome Wide Analysis and Characterization of Heat Shock Transcription Factors (Hsfs) in French Bean (Phaseolus Vulgaris L.)

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