Abstract
BackgroundThe phloem of dicotyledonous plants contains specialized P-proteins (phloem proteins) that accumulate during sieve element differentiation and remain parietally associated with the cisternae of the endoplasmic reticulum in mature sieve elements. Wounding causes P-protein filaments to accumulate at the sieve plates and block the translocation of photosynthate. Specialized, spindle-shaped P-proteins known as forisomes that undergo reversible calcium-dependent conformational changes have evolved exclusively in the Fabaceae. Recently, the molecular characterization of three genes encoding forisome components in the model legume Medicago truncatula (MtSEO1, MtSEO2 and MtSEO3; SEO = sieve element occlusion) was reported, but little is known about the molecular characteristics of P-proteins in non-Fabaceae.ResultsWe performed a comprehensive genome-wide comparative analysis by screening the M. truncatula, Glycine max, Arabidopsis thaliana, Vitis vinifera and Solanum phureja genomes, and a Malus domestica EST library for homologs of MtSEO1, MtSEO2 and MtSEO3 and identified numerous novel SEO genes in Fabaceae and even non-Fabaceae plants, which do not possess forisomes. Even in Fabaceae some SEO genes appear to not encode forisome components. All SEO genes have a similar exon-intron structure and are expressed predominantly in the phloem. Phylogenetic analysis revealed the presence of several subgroups with Fabaceae-specific subgroups containing all of the known as well as newly identified forisome component proteins. We constructed Hidden Markov Models that identified three conserved protein domains, which characterize SEO proteins when present in combination. In addition, one common and three subgroup specific protein motifs were found in the amino acid sequences of SEO proteins. SEO genes are organized in genomic clusters and the conserved synteny allowed us to identify several M. truncatula vs G. max orthologs as well as paralogs within the G. max genome.ConclusionsThe unexpected occurrence of forisome-like genes in non-Fabaceae plants may indicate that these proteins encode species-specific P-proteins, which is backed up by the phloem-specific expression profiles. The conservation of gene structure, the presence of specific motifs and domains and the genomic synteny argue for a common phylogenetic origin of forisomes and other P-proteins.
Highlights
The phloem of dicotyledonous plants contains specialized Pisum sativum (Ps)-proteins that accumulate during sieve element differentiation and remain parietally associated with the cisternae of the endoplasmic reticulum in mature sieve elements
The sieve element occlusion (SEO) gene family in Fabaceae BLAST searches were carried out using the nucleotide sequences of the three known M. truncatula SEO genes [14,15], identifying six further candidate SEO genes in the M. truncatula genome and 26 in Glycine max
In order to include all pseudogenes in subsequent phylogenetic analyses, full-length cDNA sequences were generated in silico using the procedures described in the Methods section
Summary
The phloem of dicotyledonous plants contains specialized P-proteins (phloem proteins) that accumulate during sieve element differentiation and remain parietally associated with the cisternae of the endoplasmic reticulum in mature sieve elements. The pressure-driven mass flow [2] requires plugging mechanism based on specialized phloem proteins (P-proteins) [6] These structural proteins accumulate in the cytoplasm of metabolically-active, undifferentiated SEs, but are anchored to the plasma membrane when SEs mature [7]. After wounding, they detach from their parietal location and plug downstream sieve plates by forming a gel-like mass, thereby preventing the loss of photoassimilates [8]. They detach from their parietal location and plug downstream sieve plates by forming a gel-like mass, thereby preventing the loss of photoassimilates [8] This occurs in all the dicotyledonous plant families that have been studied, and P-proteins have been identified in certain monocotyledonous plants [9]. Comprehensive promoter analyses in M. truncatula roots and Nicotiana tabacum plants demonstrated a restricted expression of the corresponding MtSEO genes in immature sieve elements [14,16], indicating a highly conserved regulation of promoter activities among diverse plant species, including non-Fabaceae lacking forisomes
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