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Lotus Japonicus and Medicago Truncatula Genetics and Molecular Biology, 35, 1 (suppl), 247-259 (2012) Copyright © 2012, Sociedade Brasileira de Genética. Printed in Brazil www.sbg.org.br Research Article Overall picture of expressed Heat Shock Factors in Glycine max, Lotus japonicus and Medicago truncatula Nina M. Soares-Cavalcanti1, Luís C. Belarmino1, Ederson A. Kido1, Valesca Pandolfi1, Francismar C. Marcelino-Guimarães2, Fabiana A. Rodrigues2, Gonçalo A.G. Pereira3 and Ana M. Benko-Iseppon1 1Departamento de Genética, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife, PE, Brazil. 2Embrapa Soja, Londrina, PR, Brazil. 3Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brazil. Abstract Heat shock (HS) leads to the activation of molecular mechanisms, known as HS-response, that prevent damage and enhance survival under stress. Plants have a flexible and specialized network of Heat Shock Factors (HSFs), which are transcription factors that induce the expression of heat shock proteins. The present work aimed to identify and characterize the Glycine max HSF repertory in the Soybean Genome Project (GENOSOJA platform), comparing them with other legumes (Medicago truncatula and Lotus japonicus) in view of current knowledge of Arabidopsis thaliana. The HSF characterization in leguminous plants led to the identification of 25, 19 and 21 candidate ESTs in soybean, Lotus and Medicago, respectively. A search in the SuperSAGE libraries revealed 68 tags distributed in seven HSF gene types. From the total number of obtained tags, more than 70% were related to root tissues (water deficit stress libraries vs. controls), indicating their role in abiotic stress responses, since the root is the first tissue to sense and respond to abiotic stress. Moreover, as heat stress is related to the pressure of dryness, a higher HSF ex- pression was expected at the water deficit libraries. On the other hand, expressive HSF candidates were obtained from the library inoculated with Asian Soybean Rust, inferring crosstalk among genes associated with abiotic and bi- otic stresses. Evolutionary relationships among sequences were consistent with different HSF classes and sub- classes. Expression profiling indicated that regulation of specific genes is associated with the stage of plant develop- ment and also with stimuli from other abiotic stresses pointing to the maintenance of HSF expression at a basal level in soybean, favoring its activation under heat-stress conditions. Key words: HSF, Fabaceae, bioinformatics, abiotic stress, transcription factor. Introduction determinant of its ability to survive a stress period (Efeoglu, Heat stress is one of the major factors limiting the 2009). However, the expression of HSF and HSP genes has productivity and adaptation of crops, especially when tem- been also observed under other abiotic and biotic stresses, perature extremes coincide with critical stages of plant de- as cited by Pirkkala et al. (2001). In response to various in- velopment. The major developmental performance of ducers such as elevated temperatures, salinity, drought, ox- plants occurs at a temperature regime between 10° and idants, heavy metals, bacterial and viral infections, most 40 °C. Temperatures below or above this range generally HSFs acquire DNA binding activity to the heat shock ele- cause temperature-induced stresses (Treshow, 1970; Hsu et ment (HSE), thereby mediating transcription of the heat al., 2010). In the case of heat stress, both the rate of temper- ature change and the duration and degree of high tempera- shock factor genes, which results in accumulation of heat tures contribute to the intensity of heat stress. The degree of shock proteins (HSPs). Among important transcription fac- inherent adaptedness to heat stress of a plant is an important tors, heat shock factors (HSFs) are essential for the tran- scription of many HSP coding genes that are active in Send correspondence to Ana M. Benko-Iseppon. Departamento de response to sublethal heat stress leading to increased toler- Genética, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Av. Prof. Morais Rego 1235, 50.670-420 Recife, PE, ance against a subsequent, otherwise lethal, heat shock Brazil. E-mail: [email protected]. (Treshow, 1970; Hsu et al., 2010). 248 Soares-Cavalcanti et al. After stress perception, intracellular changes lead to a Although the flexible network of HSF genes has been molecular cascade of events, initiated by HSF activation well studied in plants, there is little information available and subsequent expression of HSPs limiting stress damage regarding the structure and function of HSF genes in le- (Hsu et al., 2010). In general, HSF proteins have a common gumes. Additionally, no comparison of HSF orthologs has core structure comprising a N-terminal DNA binding do- been carried out until now among legumes. In this study, main (DBD) characterized by a central helix-turn-helix we used well-described Arabidopsis HSF proteins as seed (HTH) motif, an adjacent domain with a heptad hydropho- sequences in order to identify and characterize the pool of bic repeat (HR-A/B) which is involved in oligomerization, HSF genes present in the Glycine max genome and perform a short peptide motif essential for nuclear import [nuclear a comparative analysis against Lotus japonicus and localization signal (NLS)] and export [nuclear export sig- Medicago truncatula genomes, so as to trace the panorama nal (NES)], and a C-terminal AHA type activation domain of the HSF genes in these leguminous plants. (Mittal et al., 2009; Hsu et al., 2010). Through the DNA binding domain, activated HSFs Material and Methods bind to conserved cis-acting elements called heat shock ele- Based on 21 well-described Arabidopsis HSF genes ments (HSEs). HSEs are located in the promoters of HSP in the AfTDB database, BLASTp searches (Altschul et al., genes and are defined as adjacent and inverse repeats of the 1990) were carried out for similar sequences against the motif 5-nGAAn-3, for instance 5-nGAAnnTTCnnGAAn-3 GENOSOJA database. GENOSOJA connects public and (Schöffl et al., 1998). project soybean data (Nascimento et al., 2012). In total, the Some HSFs have been cloned and characterized from initiative provides information on 60,747 unigenes from various plant species (Nover et al., 2001; Baniwal et al., the NBCI, Phytozome and Soybean full-length cDNA data- 2007) revealing that the network of HSF genes is highly bases (Nascimento et al., 2012). Comparative searches flexible and specialized in this group. Details regarding the were made in the Medicago truncatula and Lotus japonicus overall HS response network were initially not clear. How- databases. After searching the GENOSOJA databank, only ever, studies in Arabidopsis revealed that 21 HSFs form a orthologs presenting the fully characteristic HSF DNA- complex network, in which AtHSFA1a and AtHSFA1b Binding Domain (DBD) were considered for subsequent play important roles in the induction of HSP genes in the analysis. In view of the obtained soybean, Medicago and early stage of HSR (Nover et al., 2001). Lotus HSF candidates together with the Arabidopsis seed- An insight into the response of HSPs and HSFs to dif- sequences, a comparative analysis with 69 aligned proteins ferent abiotic stresses was provided through a number of was performed, enabling the generation of a dendrogram, genome-wide microarray datasets. Arabidopsis HSFs and using the Neighbor-Joining (NJ) method with 2,000 boot- HSPs were strongly induced by heat, cold, salinity and os- strap replications with program MEGA program v. 5.0 (Ta- motic stresses. Furthermore, overlapping responses of mura et al., 2011), to infer about HSF groups and classes HSPs and HSFs to heat and other abiotic stresses was re- within the analyzed legumes. For this purpose the se- ported, indicating that these genes are important elements quence-coding genes from Arabidopsis that did not present in the crosstalk among different response pathways (Hu et similarity (orthology) with the studied legumes were ex- al., 2009). In rice, over-expression of OsHsp17.7 enhanced cluded from the phenetic analysis. To prevent the influence rice tolerance to heat UV-B as well as to drought (Sato and of different sequence sizes, the alignments were trimmed Yokoya, 2008). aiming to exclude unequal 5’ and 3’ extremities. Hu et al. (2009) identified rice HSF and HSP genes To evaluate the HSF-related tags represented in the and analyzed their expression profiles under different SuperSAGE libraries generated by the GENOSOJA pro- abiotic stresses. A whole-genome microarray analysis was ject, a comparative analysis using the same seed sequences carried out to investigate expression changes of rice HSFs and the MegaBLAST algorithm was carried out according and HSPs genes in response to heat stress. By comparing to Altschul et al. (1990). For this purpose the parameters their experimental data with other expression data under were adjusted to an e-value equal to or less than 0.1 and salt, cold, and drought conditions, Hu et al. (2009) found word size equal to 7. The low complexity filter was deacti- that the rice HSF and HSP families responded to different vated. Results considered only tags with identity equal to or stresses in an overlapping relationship. The analysis also larger than 23 bp. indicated that some HSF and HSP genes exhibited specific The GENOSOJA databank is comprised of six expression patterns
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