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LEA (Late Embryogenesis Abundant) Proteins and Their Encoding Genes in Arabidopsis Thaliana

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LEA (Late Embryogenesis Abundant) Proteins and Their Encoding Genes in Arabidopsis Thaliana

Michaela Hundertmark et al. BMC Genomics.

Abstract

Background: LEA (late embryogenesis abundant) proteins have first been described about 25 years ago as accumulating late in plant seed development. They were later found in vegetative plant tissues following environmental stress and also in desiccation tolerant bacteria and invertebrates. Although they are widely assumed to play crucial roles in cellular dehydration tolerance, their physiological and biochemical functions are largely unknown.

Results: We present a genome-wide analysis of LEA proteins and their encoding genes in Arabidopsis thaliana. We identified 51 LEA protein encoding genes in the Arabidopsis genome that could be classified into nine distinct groups. Expression studies were performed on all genes at different developmental stages, in different plant organs and under different stress and hormone treatments using quantitative RT-PCR. We found evidence of expression for all 51 genes. There was only little overlap between genes expressed in vegetative tissues and in seeds and expression levels were generally higher in seeds. Most genes encoding LEA proteins had abscisic acid response (ABRE) and/or low temperature response (LTRE) elements in their promoters and many genes containing the respective promoter elements were induced by abscisic acid, cold or drought. We also found that 33% of all Arabidopsis LEA protein encoding genes are arranged in tandem repeats and that 43% are part of homeologous pairs. The majority of LEA proteins were predicted to be highly hydrophilic and natively unstructured, but some were predicted to be folded.

Conclusion: The analyses indicate a wide range of sequence diversity, intracellular localizations, and expression patterns. The high fraction of retained duplicate genes and the inferred functional diversification indicate that they confer an evolutionary advantage for an organism under varying stressful environmental conditions. This comprehensive analysis will be an important starting point for future efforts to elucidate the functional role of these enigmatic proteins.

Figures

Figure 1
Figure 1
Unrooted dendrogram of all Arabidopsis LEA genes. Sequence alignments were performed unsing the ClustalW algorithm and an unrooted dendrogram was drawn subsequently. The different LEA groups are indicated by different colors, COR15A and COR15B are highlighted in the LEA_4 group.
Figure 2
Figure 2
Comparison of the sizes of the different LEA gene groups in Arabidopsis, rice (Oryza), poplar (Populus), grapevine (Vitis) and Chlamydomonas.
Figure 3
Figure 3
Alignment of the dehydrin protein sequences of Arabidopsis thaliana. Amino acid sequences were aligned using the ClustalW algorithm. Dashes indicate gaps introduced for optimal alignment. The typical dehydrin sequence elements are highlighted: K segment – red; Y segment – yellow; S segment – green; Lys-rich segment – grey. The genes forming homeologous pairs and tandem repeats in the genome (compare Fig. 6, Table 6 and 7) are indicated by arrows on the right and left side of the gene identifier, respectively. The complete sequences can also be found in Additional file 5.
Figure 4
Figure 4
Expression analysis of all 51 LEA genes in A. thaliana. Expression was measured by quantitative RT-PCR in different organs (A), in mature leaves under different stress conditions (B), in axenic cultures under hormone induction (C) and in mature seeds (D). The color coding represents relative gene expression from 0 (yellow) to 100% (red), with 100% representing the highest expression within a given panel (compare e.g. the same leaf data as represented in A and D). See Additional file 3 for the complete data set. The numbers on the sides refer to the different LEA genes that are listed in Table 1.
Figure 5
Figure 5
Plot of mean net charge versus mean hydrophobicity of LEA and selected other proteins. "No LEA" refers to proteins originally annotated as LEA proteins but re-annotated in our study (Additional file 1). Arabidopsis seed storage proteins were included in the analysis, because they are a group of seed proteins that have clearly no sequence similarities to LEA proteins. The line marks the border between natively unstructured (left) and folded (right) proteins [91]. The inset documents the shift of five proteins when the putative targeting sequence is removed.
Figure 6
Figure 6
Localization of the 51 identified LEA genes on the Arabidopsis chromosomes. Genes related by endo-reduplication events during genome evolution (homeologous genes) are connected by lines and highlighted. Genes present as tandem repeats in the genome are boxed in.

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