Emergence of Intronless Evolutionary Forms of Stress Response Genes: Possible Relation to Terrestrial Adaptation of Green Plants

摘要

The currently known gene repertoire related to terrestrialization of plants includes genes of responses to different stresses, such as UV radiation, microbial pathogen attacks, desiccation, salinity, low, and high temperature. Evolutionary details of exon-intron organization in these genes are not analyzed comprehensively, although such an analysis would be rather informative and important for understanding their evolutionary history. Particularly, a series of papers on Phragmoplastophyta stress-related intron-containing genes show their origin by horizontal gene transfer of intronless prokaryotic genes (Emiliani et al., 2009 ; Fang et al., 2017 ). The 4/1 protein is specific to plants; biochemical and cell biology data were obtained mostly for the Nicotiana tabacum 4/1 protein (Nt-4/1) (Makarova et al., 2011 ; Morozov et al., 2014 ; Atabekova et al., 2018 ). Recently, we reported that Nt-4/1 could respond to mechanical and temperature stresses by re-localization into numerous small spherical bodies likely associated with the cortical ER-plasma membrane contact sites (Atabekova et al., 2018 ). Previous studies have shown that there are some potential stress-responsive proteins among two dozen Arabidopsis and tobacco proteins interacting with 4/1 in the yeast two-hybrid system. These proteins include PBL, the ortholog of the well-characterized human ER-localized BAP31 protein; CPL, the phosphatase known to dephosphorylate the C-terminal domain of the largest subunit of DNA-dependent RNA polymerase II and involved in responses to different abiotic stress; and several stress-related transcription factors (Minina et al., 2009 ; Atabekova et al., 2017 , 2018 ; Pankratenko et al., 2017 ). Importantly, the data available in public domain microarray databases showed that expression levels of Arabidopsis and rice 4/1 genes could significantly change in response to several stress factors, particularly, anoxia, and fungal infection (Solovyev et al., 2013a ; Morozov et al., 2014 ). According to computer predictions, the secondary structure of myosin-like Nt-4/1 protein is mainly α-helical; Nt-4/1 was predicted to have six extended α-helices, and five of them represented coiled-coil structural elements (von Bargen et al., 2001 ; Makarova et al., 2011 , 2014 ; Solovyev et al., 2013b ) ( Supplementary Figure 1 ). While silencing of 4/1 gene in transgenic N. benthamiana caused no major morphological alterations in plants (Makarova et al., 2011 ; Morozov et al., 2014 ), transient virus-induced silencing of 4/1 gene in N . benthamiana resulted in faster phloem transport of Potato spindle tuber viroid (Solovyev et al., 2013a ). These data were in line with our findings showing that at the 4/1 promoter is active in veins, with its activity being detected mostly in xylem parenchyma, phloem parenchyma, and primary phloem cells (Solovyev et al., 2013a ). Organ- and tissue-specific expression patterns of some other plant 4/1 genes in public microarray databases were found to be consistent with 4/1 expression in conductive tissues (Solovyev et al., 2013a ; Morozov et al., 2014 ). Thus, we proposed that the 4/1 protein could influence stress signaling in the vasculature (Atabekova et al., 2018 ). The 4/1 genes encoded by the genomes of genera Arabidopsis and Nicotiana were shown to contain eight exons and seven introns (Paape et al., 2006 ; Makarova et al., 2011 ). A similar exon-intron structure was found for most 4/1 genes encoded by other dicotyledonous and monocotyledonous plants with some notable exceptions (Morozov et al., 2015 ) ( Figure 1 ). To better understand the evolution of 4/1 genes, a comparative analysis of these genes in lower land plants in combination with structural analysis of encoded proteins was carried out. We have partially or completely sequenced 4/1 genes of some representatives of liverworts, Lycopodiopsida, ferns, and gymnosperms (Morozov et al., 2015 ). Interestingly, using publicly available databases containing next generation sequencing data, we were unable to identify 4/1-specific signatures in genomes of mosses Physcomitrella patens (class Bryopsida) and Sphagnum fallax (class Sphagnopsida). However, we reported that the genomes of basal land plants Marchantia polymorpha (class Marchantiopsida) and Anthoceros agrestis (class Anthocerotopsida) as well as partial assembled charophyte cDNA sequences from Chaetosphaeridium globosum (class Coleochaetophyceae) and several species of class Zygnematophyceae (including Spirogyra pratensis ), could encode proteins similar to 4/1 proteins of Magnoliophyta (Morozov et al., 2014 , 2015 ). Importantly, our efforts to reveal 4/1-like genes in basal charophyte classes Klebsormidiophyceae (Hori et al., 2014 ) and Chlorokybophyceae as well as in all moss classes, failed (Morozov et al., 2015 ). Figure 1 The exon/intron structure of selected plant stress-related genes in representatives of different taxa. Exons are indicated by boxes, and introns are indicated by li