Genome-wide analysis of the omega-3 fatty acid desaturase gene family in Gossypium
© Yurchenko et al.; licensee BioMed Central Ltd. 2014
Received: 26 June 2014
Accepted: 28 October 2014
Published: 18 November 2014
The majority of commercial cotton varieties planted worldwide are derived from Gossypium hirsutum, which is a naturally occurring allotetraploid produced by interspecific hybridization of A- and D-genome diploid progenitor species. While most cotton species are adapted to warm, semi-arid tropical and subtropical regions, and thus perform well in these geographical areas, cotton seedlings are sensitive to cold temperature, which can significantly reduce crop yields. One of the common biochemical responses of plants to cold temperatures is an increase in omega-3 fatty acids, which protects cellular function by maintaining membrane integrity. The purpose of our study was to identify and characterize the omega-3 fatty acid desaturase (FAD) gene family in G. hirsutum, with an emphasis on identifying omega-3 FADs involved in cold temperature adaptation.
Eleven omega-3 FAD genes were identified in G. hirsutum, and characterization of the gene family in extant A and D diploid species (G. herbaceum and G. raimondii, respectively) allowed for unambiguous genome assignment of all homoeologs in tetraploid G. hirsutum. The omega-3 FAD family of cotton includes five distinct genes, two of which encode endoplasmic reticulum-type enzymes (FAD3-1 and FAD3-2) and three that encode chloroplast-type enzymes (FAD7/8-1, FAD7/8-2, and FAD7/8-3). The FAD3-2 gene was duplicated in the A genome progenitor species after the evolutionary split from the D progenitor, but before the interspecific hybridization event that gave rise to modern tetraploid cotton. RNA-seq analysis revealed conserved, gene-specific expression patterns in various organs and cell types and semi-quantitative RT-PCR further revealed that FAD7/8-1 was specifically induced during cold temperature treatment of G. hirsutum seedlings.
The omega-3 FAD gene family in cotton was characterized at the genome-wide level in three species, showing relatively ancient establishment of the gene family prior to the split of A and D diploid progenitor species. The FAD genes are differentially expressed in various organs and cell types, including fiber, and expression of the FAD7/8-1 gene was induced by cold temperature. Collectively, these data define the genetic and functional genomic properties of this important gene family in cotton and provide a foundation for future efforts to improve cotton abiotic stress tolerance through molecular breeding approaches.
KeywordsChilling tolerance Cotton Drought Fatty acid desaturase Gossypium Linolenic acid Omega-3 fatty acid
Cotton is an important crop worldwide, providing the majority of fiber to the textile industry and a significant amount of oilseed for food, feed, and biofuel purposes. The most commonly grown cotton species for commercial production is Gossypium hirsutum, an allotetraploid species with a remarkable evolutionary history. The cotton genus (Gossypium) originated approximately 12 million years ago (MYA)  and underwent rapid radiation and adaptation to many arid or seasonally arid tropical or subtropical regions of the world ,. Despite a wide range of morphological phenotypes, including trees and bushes, cytogenetic and karyotyping analyses revealed that the majority of plants can be categorized as having 1 of 8 distinct types of diploid genomes (n = 13) . The A, B, E, and F genome-containing plants are found in Africa and Arabia, the C, G, and K genomes are common to Australian plants, and the D genome-containing species are found in Mesoamerica. G. hirsutum is an AD tetraploid also found predominantly in Mesoamerica, which suggests that this species arose by trans-oceanic dispersal of A-type seed from Africa, followed by chance interspecific hybridization with a D-containing progenitor species in the New World ,. Molecular systematics studies suggest that the A and D diploid species evolved separately for approximately 5–10 million years before being reunited in the same nucleus approximately 1–2 MYA . G. hirsutum (the source of upland cotton) was subsequently domesticated for fiber production in the last few thousand years in the New World, and as such, is an interesting model system not only for use in the study of genome evolution, but also for studying the role of polyploidy in crop development and domestication .
Given that G. hirsutum is native to the tropics and subtropics, it is adapted to the warm temperatures of arid and semi-arid climates ,. In the US, upland cotton is planted at various times throughout the year and the beginning and end of the growing seasons often include sub-optimal growth temperatures and environmental conditions. For instance, heat and drought can cause significant reductions in crop yield during the latter parts of the growing season ,. Exposure of cotton to sudden episodes of cold temperature during the early parts of the growing season, moreover, can cause significant damage to cotton seedlings and the plants may not fully recover -. Development of upland cotton varieties with improved tolerance to low temperature stress could thus improve the agronomic performance of the crop and thereby significantly impact the cotton industry ,.
The adaptation of plants to low temperature is a complex biological process that involves changes in expression of many different genes and alteration in many different metabolites -. One of the common biochemical responses in plants to cold temperature is an increase in relative content of polyunsaturated fatty acids (PUFAs) -. Polyunsaturated fatty acids have a lower melting temperature than saturated and monounsaturated fatty acids, and their increased accumulation is thought to help maintain membrane fluidity and cellular integrity at cold temperatures . For instance, cold temperature treatment of cotton seedlings has been shown to induce the accumulation of PUFAs ,, and inclusion of an inhibitor of PUFA biosynthesis during the treatment rendered the seedlings more susceptible to cold temperature damage . By contrast, warm temperatures were inversely associated with PUFA content and changed during leaf expansion, and this impacted photosynthetic performance of cotton plants in the field . Thus, gaining a better understanding of the genes that regulate PUFA production in cotton represents a first step in improving cold and thermotolerance in upland cotton germplasm.
The metabolic pathways for PUFA production in plants are generally well understood and have been elucidated primarily by studying various fatty acid desaturase, or fad mutants, of Arabidopsis that are blocked at various steps of lipid metabolism . Briefly, fatty acid biosynthesis occurs in the plastids of plant cells, with a successive concatenation of 2 carbon units resulting in production of the 16- or 18-carbon long fatty acids that predominate in cellular membranes. A soluble fatty acid desaturase is present in the plastid stroma for conversion of 18:0 into 18:1, where the number before the colon represents the total number of carbons in the fatty acid chain and the number after the colon indicates the number of double bonds. The 18:1 fatty acid is subsequently available for further desaturation by one of two parallel pathways operating in either the plastid or endoplasmic reticulum (ER). For instance, 18:1 may be converted to 18:2 in plastids by a membrane-bound fatty acid desaturase called FAD6, or the 18:1 may be exported from the plastids to the ER for conversion to 18:2 by a structurally related enzyme called FAD2. The FAD2 and FAD6 enzymes are similar at the polypeptide sequence level, with the exception that the FAD6 protein contains a longer N-terminal sequence that is characteristic of a chloroplast transit peptide. In a similar fashion, 18:2 may be converted into 18:3 in plastids by the FAD7 or FAD8 enzymes, which are encoded by two closely related genes in Arabidopsis, or can be exported to the ER for conversion to 18:3 by the FAD3 enzyme. This latter group of enzymes (FAD7/FAD8 and FAD3) are referred to as omega-3 fatty acid desaturases, since they introduce a double bond at the omega-3 position of the fatty acid structure. Thus the FAD6 and FAD2 enzymes, which produce 18:2, and the FAD7/FAD8 and FAD3 enzymes, which produce 18:3, all play central roles in production of the PUFAs that are present in all plant species.
Knowledge of the FAD genes encoding these enzymes has permitted more detailed analyses of the role of these genes, and their fatty acid products, in plant lipid metabolism and abiotic stress response. For instance, omega-3 fatty acids are known to increase in plants in response to both drought , and cold temperature -, and over-expression of omega-3 desaturases in various transgenic plants has been shown to improve both drought and chilling tolerance -. The ER-localized desaturases FAD2 and FAD3 are also involved in production of PUFA components of seed oils , and given the importance of these fatty acids to human nutrition, and to determining stability of oils during cooking or other food applications, molecular markers for these genes have been developed for evaluating germplasm and identifying oilseed varieties with improved oil compositions -.
Given the prominent role of PUFAs in chilling and drought adaptation of plants, and the susceptibility of cotton seedlings to both of these environmental conditions, we sought to identify and characterize the genes involved in PUFA synthesis in cotton. Since several FAD2 genes have been previously reported and characterized in cotton -, we chose instead to focus on the analysis of the omega-3 FAD gene family, of which no members have been previously studied. Here we describe the complete omega-3 gene family in both tetraploid G. hirsutum as well as extant A and D diploid progenitor species (G. herbaceum and G. raimondii, respectively), which allowed clear assignment of all homoeologous genes. We also describe organ and cell-type specific gene expression patterns, and identify a single FAD7/FAD8-type gene that is inducible by both drought as well as cold-temperature exposure of cotton seedlings. Collectively, these data define the content and functional genomic properties of this important gene family in commercial upland cotton.
Results and discussion
Identification and phylogenetic analysis of the omega-FAD gene family in cotton
The omega-3 FAD-type genes in G. hirsutum (AD1 allotetraploid), G. herbaceum (A1 diploid), and G. raimondii (D5 diploid) were cloned and sequenced using a combination of database mining, degenerate primer-based PCR screening, genome resequencing, and gene-specific PCR-based cloning, as described in the Methods. All cloning, DNA sequencing, and RT-PCR primer sequences are provided in Additional files 1, 2, and 3, respectively. During the cloning process, the genome sequence of G. raimondii (D5) was released , which confirmed the identity of omega-3 genes we had identified in this organism. The perfect match between our cloned gene sequences and the genes in the genome database provided a useful check for the fidelity of the cloning process employed here. More recently, a draft of the genome sequence of G. arboreum (A2) was released , which will enable future studies aimed at comparing gene sequences between A genome-containing species.
Summary of omega-3 FAD genes cloned from cotton
RNA-seq analysis of gene expression patterns
Taken together, these data define organ and cell-type specific gene expression patterns for various members of the omega-3 fatty acid desaturase gene family in G. hirsutum, with FAD3-1 expressed predominantly in fibers, FAD7/8-2 in leaves, and FAD7/8-1 induced by drought treatment in cotton roots.
FAD7/8-1 expression is induced in cotton seedlings in response to cold temperature
To investigate gene expression patterns in cold-treated G. hirsutum seedlings, we first developed gene-specific PCR primers capable of distinguishing each omega-3 FAD homoeolog. We chose to develop PCR-based strategies rather than RNA-seq for monitoring gene expression since the PCR primers developed herein can be used also for future candidate gene association mapping studies. The goal of such mapping studies is to test whether sequence variants (e.g., single-nucleotide polymorphisms, SNPs) at candidate genes are statistically associated with a particular trait (e.g., chilling tolerance) in a panel of diverse lines ,. To develop homoeolog-specific primers, we first aligned the respective omega-3 FAD genes to identify SNPs and insertions-deletions (indels) that were specific to each gene (Additional files 5, 6, 7, 8 and 9). Our general strategy for designing primers was that each primer pair should amplify a fragment of approximately 500 bp from mRNA, and the 3′-most nucleotide of each primer should be unique to each homoeolog. The specificity of each primer set was tested and optimized using gradient PCR annealing conditions and plasmid DNA templates containing either the target homoeolog, or the most closely related sequence. In some cases, the primers amplified both homoeologs and needed redesigning for improved specificity. The final sets of primers capable of distinguishing each homoeolog are listed in Additional file 3. Primer optimization experiments for FAD3-type genes are presented in Additional file 11, and FAD7/8-type genes are shown in Additional file 12.
Five omega-3 FAD-type genes were identified in cotton, two of which encode ER-localized enzymes (FAD3-1 and FAD3-2) and three that encode chloroplast-type enzymes (FAD7/8-1, FAD7/8-2 and FAD7/8-3) (Table 1; Figure 1). Phylogenetic analysis revealed that the genes could be grouped into three major clades (Figure 2), the first of which contained all FAD3-type genes. Functional analysis revealed that the FAD3-1 gene is predominantly expressed in elongating cotton fibers (Figure 3) and likely contributes to the synthesis of linolenic acid, the most abundant fatty acid in fibers. The FAD3-2 gene is expressed at a relatively low level in all conditions examined here, and is duplicated in the A genome of G. herbaceum and A subgenome of G. hirsutum. This latter paralog also contains several in-frame stop codons (Additional file 6). Given the low expression of FAD3-2 compared to FAD3-1, it seems likely that FAD3-1 plays a more dominant role in production of linolenic acid in the ER of cotton cells. Clade 2 contains the FAD7/8-1 and FAD7/8-3 genes (Figure 2), and RNA-seq and semi-quantitative RT-PCR showed that FAD7/8-1 is induced by abiotic stress, including drought treatment in roots (Figure 5B), and cold treatment in cotton leaves (Figure 7E and F). The FAD7/8-3 gene is expressed at a relatively low level in all experiments described here and includes a substitution mutation in a highly conserved region of the encoded polypeptide sequence (Figure 1). The third clade includes the FAD7/8-2 gene, which likely serves more of a housekeeping role for production of 18:3 in cotyledons (Additional file 12B), leaves (Figure 4 and Additional file 10D), and petals (Figure 4 and Additional file 10C). Unlike FAD7/8-1, the FAD7/8-2 gene did not show pronounced induction by abiotic stress in response to either drought (Figure 5A) or cold temperature treatment (Figure 7E and F). Notably, the Arabidopsis FAD7 and FAD8 genes also show differential response to chilling treatment, with FAD7 expression unaffected by cold temperature  while FAD8 expression is induced at low temperature . Taken together, these data define the evolutionary and functional properties of the omega-3 FAD gene family in cotton and identify specific members of the gene family associated with fiber biogenesis and abiotic stress response.
Gene cloning and annotation
For the initial search of omega-3 FAD genes in cotton, we employed several different approaches including i) BLAST analysis of extant Gossypium sequences in various genome databases (e.g., NCBI, CottonDB, Phytozome) using Arabidopsis thaliana omega-3 desaturases as queries; ii) PCR-based screening of cotton genomic DNA and cDNA libraries using “degenerate” PCR primers corresponding to conserved regions of omega-3 fatty acid polypeptide sequences; and iii) PCR amplification using gene-specific primers (see Additional file 1 for primer sequences). Genomic DNA from G. herbaceum, G. raimondii, G. hirsutum, and G. barbadense was used as templates in PCR reactions. Additional insight to the omega-3 FAD gene family was obtained with the release of the genome sequence for the diploid progenitor G. raimondii .
Our preliminary analysis identified five different omega-3 desaturase genes in cotton, including two genes encoding putative endoplasmic reticulum-localized enzyme (FAD3-1 and FAD3-2), and three genes encoding putative chloroplast-localized enzymes (FAD7/8-1, FAD7/8-2, FAD7/8-3). Each of the five genes was subsequently cloned and sequenced from two progenitor-type cotton species, G. herbaceum (A genome; PI 175456) and G. raimondii (D genome; PI 530901), as well as from modern upland cotton, G. hirsutum TM1 (AD tetraploid; PI 662944 MAP; ). To ensure fidelity of cloned gene sequences, the following strategy was employed. Gene-specific PCR primers were designed to hybridize in the 5′ and 3′ UTR regions near the start and stop codons, respectively, and used in PCR reactions containing genomic DNA isolated from a single plant from each species. The PCR reaction was divided into three aliquots that were each subjected to PCR amplification using a gradient of annealing temperatures, and extension times appropriate for each gene. The high fidelity polymerase “Phusion” (New England Biolabs, Ipswich, MA) was used for amplification. PCR products were resolved on DNA gels and bands of expected size were extracted and purified using the GeneClean kit (MP Biomedicals, Santa Ana, CA) and ligated into appropriate plasmid vectors. In some cases, blunt-ended PCR products were subcloned into pZero-Blunt (Life Technologies, Carlsbad, CA), while in other cases, unique restrictions sites were added to the 5’ and 3’ ends of gene-specific primers to allow for directional subcloning into pUC19.
Ten individual plasmids derived from each of the three initial PCR reactions for a single gene (30 plasmids total), were subject to DNA sequencing (Retrogen, Inc., San Diego, CA), with DNA sequences determined in both the forward and reverse directions (see Additional file 2 for sequencing primers). Full-length gene sequences were assembled using the ContigExpress module of Vector NTI (v 11.0; Life Technologies, Grand Island, NY). The sequences of all thirty plasmids representing a single gene target were aligned to help identify sequencing artifacts, PCR-based artifacts, and gene sequences resulting from PCR-based recombination. The latter artifact is quite common when amplifying a gene from a polyploid plant, such as G. hirsutum , and involves essentially random crossing over of homoeologous sequence templates during PCR amplification. Knowledge of the omega-3 FAD gene sequences from the diploid progenitor species was essential for helping to determine the homoeologous gene sequences in tetraploid G. hirsutum. Intron/exon assignments were determined by aligning the genomic sequences with cotton FAD cDNAs or ESTs, if available, or predicting splice sites using algorithms available at www.softberry.com and comparison to well characterized sequences of Arabidopsis omega-3 desaturases. All of the gene sequences, as well as putative mRNA sequences, from G. herbaceum, G. raimondii, and G. hirsutum were deposited in GenBank and accession numbers are provided in Additional file 4.
The 22 full-length omega-3 FAD gene sequences identified in this study, as well as 3 homologous sequences from the T. cacao genome (Additional file 4) were aligned with T-Coffee (v10.0; ) using default parameters. The multiple sequence alignment was subsequently cleaned using Gblocks  to remove poorly aligned and predominantly gap-containing regions, using the following parameters: a minimum of 15 sequences were required for a conserved position and a flank position, no limit was placed on the number of contiguous nonconserved positions, at least two nucleotides were required for a conserved block, and gaps were allowed in at most 14 taxa at a given position. An unrooted phylogenetic tree was generated using the maximum likelihood method implemented in the online version of the PhyML program (http://www.atgc-montpellier.fr/phyml v3.0; ) using a BioNJ  initial tree and a GTR + gamma nucleotide substitution model with parameters inferred from the data. Branch support was estimated using the aLRT method . The tree was visualized and annotated using FigTree (v1.4; http://tree.bio.ed.ac.uk/software/figtree). For visualization purposes, the tree was mid-point rooted.
Evaluation of gene expression using RNA-seq and semi-quantitative RT-PCR
RNA-seq measurements of gene expression were mined from several cotton RNA-seq studies ,, that sampled fiber, leaf, and petal tissues. RNA-seq expression levels of the FAD genes in developing seeds were obtained from R. Hovav and J. Wendel (personal communication). RNA-seq data for the drought experiment were obtained from . The omega-3 FAD genes identified in this study were aligned against the D-genome reference sequence  using GSNAP  in order to identify the corresponding gene models, and RPKM (reads per kilobase per million mapped reads) measurements corresponding to the appropriate gene model were extracted from the published data.
For semi-quantitative RT-PCR, gene-specific primers were designed by aligning the homoeologous sequences of omega-3 desaturases from G. hirsutum to identify SNPs and indels that were specific to each gene (see Additional files 5, 6, 7, 8 and 9). The specificity of primer binding was then evaluated using PCR and plasmid templates harboring either the target gene or the closest related homoeolog. Optimal annealing temperatures for each primer pair were determined using gradient annealing PCR conditions. In some cases, amplification was observed using both plasmid templates, at all annealing temperatures, and primers were subsequently re-designed to bind to other gene-specific regions and specificity tested. All final primer sets showed homoeolog-specific amplification from plasmid DNA templates at the indicated optimal annealing temperatures (see Additional files 11 and 12).
To evaluate transcript abundance using RT-PCR, total RNA was extracted from frozen leaf tissue using the Spectrum Plant Total RNA Kit (Sigma-Aldrich, St. Louis, MO) then cDNA was constructed using 1 μg of total RNA and the iScript kit, as described by the manufacturer (Bio-Rad, Hercules, CA). Additional reactions were set up with iScript RT supermix, but without reverse transcriptase, to control for potential genomic DNA contamination. Semi-quantitative PCR was conducted using Extract-N-Amp PCR Ready Mix (Sigma-Aldrich) programmed with 1 μl of cDNA template (corresponding to 50 ng of RNA/cDNA) and each FAD gene primer pair, or 0.1 μl of cDNA template (corresponding to 5 ng of RNA/cDNA) and actin gene primers. These amounts of plasmid DNA template, as well as number of cycles, were determined empirically for each gene to ensure that amplification was within the linear range. The PCR included the following program conditions: initial hold at 98°C for 30 sec, then 30 cycles of denaturation at 95°C for 10 sec, annealing at the appropriate Tm for each primer pair (determined as described above) for 30 sec, then extension at 72°C for the period determined for each PCR product. After the 30th cycle, reactions were incubated at 72°C for an additional 5 min to complete extension then held at 4°C, followed by storage at −20°C. Four μl of 6X loading dye was added to the 20 μl PCR reactions, then 10 μl of each sample was analyzed by agarose gel electrophoresis and ethidium bromide staining. Gel images were captured using a FUJI LAS-4000 imaging system and band intensities were quantified using MultiGauge V3.1 software.
Plant growth conditions and sample collections
Cotton seeds were planted in damp soil in 24×16×16 plastic pots (1 seed per pot), covered with a plastic dome, and placed in a growth chamber programmed with a 12 h/12 h day/night cycle at 30°C, 60% relative humidity, and 2.14 Kfc light intensity. Plants were watered twice a week, and fertilized with 20-20-20 once a week. 13-day-old plants were subjected to chilling treatment (10°C) at the beginning of the 14th light/dark cycle. The control group of plants remained at 30°C for the 14th cycle. The first true leaf was collected at 0, 1, 3, 6, 12, 18 and 24 h after the start of the cold treatment for both treatment and control groups and immediately frozen in liquid nitrogen and stored at −80°C until used. Three biological reps were collected for each time point.
Lipid extraction and GC/FID analysis
Total lipids were extracted from the leaf tissues using a modified Bligh and Dyer method . Briefly, frozen leaves were placed in a glass tube with 3 ml of preheated (75°C) isopropanol and incubated for 15 min. After the samples cooled to room temperature, 1.5 ml of chloroform and 0.6 ml of water were added. The samples were vigorously shaken, and the lipids were extracted for 1 h at RT. The extracts were transferred to clean glass tubes. To these, 1.5 ml of chloroform and 1.5 ml of 1 M KCl were added, and the samples were vigorously shaken. After centrifugation at 3,000 rpm for 3 min the upper phase was discarded and the organic phase was washed once with 2 ml of water. After centrifugation at 3,000 rpm for 3 min the organic (bottom) phase was transferred to a clean tube, dried down under a gentle stream of nitrogen and used for FA transmethylation. 1 ml of methanol HCl (1.25 M) was added to the dried lipid extract. Samples were vortexed and incubated at 80°C for 1 h. Tubes were allowed to cool to room temperature and reactions were terminated with 1 ml of 0.9% NaCl aqueous solution. After addition of 1 ml of hexane the samples were shaken, then centrifuged at 1000 × g for 1 min to facilitate the phase separation. The upper phase (organic) containing FAMEs was transferred to GC vials. FAME samples were analyzed using an Agilent HP 6890 Series GC system equipped with 7683 Series Injector and autosampler. FAME samples were injected on BPX70 (SGE Analytical Science, Ringwood Victoria, Australia) capillary column (10 m 0.1 mm × 0.2 um) with 50:1 split ratio and separated with constant pressure 25 psi and a temperature program: hold at 145°C for 5 min, 145–175°C at 2°C/min, hold 175°C for 1 min, 175–250°C at 30°C/min. Integration events were detected between 9 and 20 min and identified by comparing to GLC-10 FAME standard mix (Sigma).
All accession numbers for genes described in this study are provided in Additional file 4.
Availability of supporting data
The sequence data supporting the results of this article are available in the GenBank [GenBank; Gossypium species: KF460111-KF460114, KF460117-KF460154, KF572120-KF572121; http://www.ncbi.nlm.nih.gov/genbank/] and Phytozome [Phytozome; Arabidopsis thaliana: AT2G29980.1, AT3G11170.1, AT5G05580.1; Theobroma cacao: Thecc1EG041603t1, Thecc1EG021677t1, Thecc1EG042487t1; http://www.phytozome.net/] repositories. The phylogenetic datasets are available at the LabArchives repository [http://dx.doi.org/10.6070/H4WS8R7Q].
This work was supported by the U. S. Department of Energy, BER Division (Grant No. DE-FG02-09ER64812/DE-SC0000797) to KDC and JMD, USDA-NIFA/DOE Biomass Research and Development Initiative (BRDI) Grant No. 2012–10006 to MAG and MAJ, NSF (0817707) and Cotton Inc. (09–559) grants to JAU, and Cotton Inc. grant 12–157 to JMD. The authors thank Saumya Bollam, T.J. Lentz, Judy Nguyen, and Lauren Tomlin for assistance with gene cloning.
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