The wild strawberry kinome: identification, classification and transcript profiling of protein kinases during development and in response to gray mold infection

- Background: Protein kinases (PKs) play an important role in signaling cascades and are one of the largest and most conserved protein super families in plants.
- Despite their importance, the woodland strawberry (Fragaria vesca) kinome and expression patterns of PK genes remain to be characterized..
- Almost half of the putative PKs were predicted to localize to the nucleus and 24.6% were predicted to localize to the cell membrane.
- The expansion of the woodland strawberry PK gene family occurred via different duplication mechanisms and tandem duplicates occurred relatively late as compared to other duplication types.
- Conclusions: The findings of this research expand the understanding of the evolutionary dynamics of PK genes in plant species and provide a potential link between cell signaling pathways and pathogen attack..
- Protein kinases (PK) are a large and widely distributed pro- tein superfamily found in prokaryotes and eukaryotes and comprise one of the largest and most conserved protein gene super-families in plants.
- For example, in humans, PKs only account for 1.7% of the coding sequence [9] whereas in Arabidopsis and rice, they account for ~ 4.
- 3 Department of Plant Sciences, University of Tennessee, Knoxville 37996, USA Full list of author information is available at the end of the article.
- Woodland strawberry (Fragaria vesca.
- Rosacea) is one of the most widely distributed indigenous species in the northern hemisphere [13].
- As one of the progenitors of the cultivated octoploid strawberry, Fragaria × ananassa [14], it serves as a model for this economically important species.
- The genome of the woodland strawberry is ~ 240 Mb in size with seven pairs of chromosomes (2n = 2x = 14) [15].
- Some woodland strawberry PK genes have been characterized and shown to be involved in abi- otic and biotic stress responses including MAPKs [16], AMP-activated protein kinase (AMPK) [17], leucine-rich repeat receptor-like protein kinase (LRR-RLK) [18], and calcium-dependent protein kinase (CDPK) [19]..
- We determined the structure and chromosomal distribution of the PK genes, as well as made predictions on the subcellular localization of the putative PK proteins.
- Thus, we present a comprehensive analysis of the PK genes found in the woodland strawberry genome and their developmental expression patterns and responses to biotic stress..
- Genome-wide identification and classification of protein kinases in woodland strawberry.
- Out of all the groups, the RLK group had the most members, which accounted for 67.0% of the total PK genes.
- The properties of woodland strawberry kinome.
- Out of the 954 PK genes lacked introns.
- In others of the PKs contained more than ten introns, while 34 (3.6%) others contained more than 20 introns.
- Among 34 members in the STE_STE11 family, 11 were intronless, whereas each of the remaining 23 family members con- tained four to 30 introns.
- Based on the phylogenetic rela- tionships of these genes in the STE_STE11 family, all of the members could be clearly divided into two clusters based on the number of introns-clusters without introns and clusters that are intron-rich (>.
- To gain further insights into the potential functions of the woodland strawberry PK proteins, the subcellular localization of each amino acid translation was predicted using Plant-mPLoc.
- The result indicated that 58.4% of the PKs were predicted to localize to the nucleus and 24.6% were predicted to localize to the cell membrane (Fig.
- Different duplication types among woodland strawberry PKs.
- The woodland strawberry kinome had 78 WGD events with 145 PK genes, that involved 90 RLK kinase genes (Additional file 7:.
- Additional file 7: Table S6 shows different duplication patterns drove the expansion of woodland strawberry PK genes..
- In order to estimate the time of different duplication types in the PK genes, synonymous substitution (Ks) rates of the duplicated gene pairs were determined.
- 1 The predicted subcellular localization of woodland strawberry protein kinases in each kinase group.
- Expression patterns of woodland strawberry PKs in different tissues during development.
- In order to explore the expression patterns of strawberry PK genes in different tissues, an in silico analysis of the transcriptomic data from carpel, anther, cortex, embryo, ghost, leaf, ovule, pith, pollen, seedling, style, wall, micro- spores, flowers, perianth, and receptacle was conducted [23].
- Based on the heatmap cluster analysis of PK expres- sion, the 952 woodland strawberry PK genes were classified into eight clusters (Fig.
- The GO analysis of the PKs in each cluster supported the results.
- The woodland strawberry PKs in cluster 1–6 were all enriched in GO terms of “recognition of pollen” (Add- itional file 17: Figure S10).
- The bars at the top and bottom of the whiskers mean maximum and minimum values.
- the top and bottom of the box represent third and first quartiles.
- 4 Chromosomal locations of all the kinase genes in woodland strawberry.
- RNA-seq analyses of woodland strawberry PK genes in response to gray mold infection.
- However, most woodland strawberry PK genes in cluster 3 showed little changes and variations comparing with the control upon B.
- The RLK group is the largest group of PKs in woodland strawberry kinome.
- 2% of its genome, and almost 61% of the Arabidopsis kinome [26].
- The proportion of RLKs is also over 50% of the kinome in other species including pine- apple (63.3.
- In this study, a total of 639 RLK genes were identified, accounting for about 67% of the woodland strawberry kinome, which is consistent with the species mentioned above.
- Among these kinase families of the strawberry RLK families contained more than ten members.
- Different duplication patterns drive the expansion of woodland strawberry kinome.
- Segmental duplication events were the main cause for the expansion of the soybean kinome [3].
- Segmental, tandem, or whole-genome duplication events have been key in the expansion of the gene families in both the grapevine and pineapple kinomes, especially in the RLK group [27, 28]..
- Environmental pressure can promote the divergence of du- plicated genes, to adapt to dramatic environmental changes because of the frequent occurrence of transposed duplica- tion [30].
- PKs) events also played critical roles in the expansion of the strawberry PKs.
- In contrast to WGD, tandem du- plications have taken place much more frequently and are responsible for more of the gene copy number and allelic variation within a population [33].
- Most of the strawberry PK tandem duplications had a Ka/Ks <.
- Most of the recent expansion of the Arabi- dopsis RLK genes were reported to be associated with defense/resistance responses [26].
- In this study, 88 of the PK genes belonged to the RLK group (Additional file 18-19: Figure S11-12), suggesting that members of this group play a.
- major role in the woodland strawberry response to this pathogen.
- This is consistent with the fact that woodland strawberry RLK members were predicted to be.
- 9 A heatmap of the expression data of all the strawberry kinase genes in response to gray mold.
- Previous studies reported that pathogen recognition were linked to transcriptional reprogramming by CDPK/CPK and MAPK cascades [36–38], and the genes reported here will be of inter- est to elucidate and characterize the underlying bio- chemistry and molecular biology of the disease response in woodland strawberry..
- Almost half of the PKs were predicted to localize to the nucleus and membrane.
- Identification and classification of woodland strawberry protein kinases.
- The predicted proteome for the woodland strawberry was downloaded from Phytozome v12.1 [39].
- To improve the accuracy of the putative predictions, the presence of a kinase domain in each of the candidate PK genes was verified using Pfam and SMART [41].
- Full-length amino acid translations of the woodland strawberry PK genes were aligned using MUSCLE in MEGA X using default settings [42].
- The chromosomal positions of the predicted PK genes were retrieved from the woodland strawberry database [39], and their locations were mapped to the corre- sponding chromosomes using MapChart v2.3 software [45].
- Identification of gene duplication events in woodland strawberry kinome.
- The transposed duplication pairs had to meet the condition of one member of the pair had to exist at the ancestral locus and the other at a non-ancestral locus [21]..
- GO analysis of PK genes in woodland strawberry.
- The false discovery rate (FDR) ≤0.01 and an absolute value of the | logFC | ≥2 were used as thresholds to evaluate the significance of gene expression differences..
- cinereal with respect to time, we con- ducted a similar analysis of the expression data from mature strawberry fruits infected with B.
- Kinase domain annotation of typical woodland strawberry protein kinases..
- A heatmap of the expression data of strawberry kinase genes in cluster 1 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 2 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 3 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 4 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 5 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 6 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 7 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of strawberry kinase genes in cluster 8 in 16 different strawberry tissues and developmental stages..
- A heatmap of the expression data of the strawberry kinase genes in cluster 1 response to gray mold..
- A heatmap of the expression data of the strawberry kinase genes in cluster 2 response to gray mold..
- A heatmap of the expression data of the strawberry kinase genes in cluster 3 response to gray mold..
- All authors contributed to modification of the MS.
- This work was supported by the open funds of the State Key Laboratory of Crop Genetics and Germplasm Enhancement (ZW201813)..
- Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
- Genome-wide classification, evolutionary analysis and gene expression patterns of the kinome in Gossypium.
- The protein kinase complement of the human genome.
- Diversity, classification and function of the plant protein kinase superfamily.
- Genome re-annotation of the wild strawberry Fragaria vesca using extensive Illumina-and SMRT-based RNA-seq datasets.
- Genome-wide characterization and expression analysis of sugar transporter family genes in woodland strawberry.
- The genome of woodland strawberry (Fragaria vesca).
- identification and transcript profile analysis of the mitogen-activated protein kinase gene family in the diploid woodland strawberry Fragaria vesca.
- Genome-wide characterization, evolution, and expression analysis of the leucine-rich repeat receptor-like protein kinase (LRR-RLK) gene family in Rosaceae genomes.
- Evolution of the R2R3-MYB gene family in six Rosaceae species and expression in woodland strawberry..
- Genome-scale Transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca.
- Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.
- Divergent evolutionary patterns of the MAPK cascade genes in Brassica rapa and plant phylogenetics.
- Genome-wide analysis and evolution of the bZIP transcription factor gene family in six Fragaria species.
- Loss or duplication of key regulatory genes coincides with environmental adaptation of the stomatal complex in Nymphaea colorata and Kalanchoe laxiflora.
- Re-annotation of the woodland strawberry (Fragaria vesca) genome.
- an online genomic resource for the woodland strawberry.
- Floral Transcriptomes in woodland strawberry uncover developing receptacle and anther gene networks

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