Polymorphism and structure of style–specific arabinogalactan proteins as determinants of pollen tube growth in Nicotiana

BACKGROUND: Pollen tube growth and fertilization are key processes in angiosperm sexual reproduction. The transmitting tract (TT) of Nicotiana tabacum controls pollen tube growth in part by secreting pistil extensin-like protein III (PELPIII), transmitting-tract-specific (TTS) protein and 120 kDa glycoprotein (120 K) into the stylar extracellular matrix. The three arabinogalactan proteins (AGP) are referred to as stylar AGPs and are the focus of this research. The transmitting tract regulates pollen tube growth, promoting fertilization or rejecting pollen tubes. RESULTS: The N-terminal domain (NTD) of the stylar AGPs is proline rich and polymorphic among Nicotiana spp. The NTD was predicted to be mainly an intrinsically disordered region (IDR), making it a candidate for protein-protein interactions. The NTD is also the location for the majority of the predicted O-glycosylation sites that were variable among Nicotiana spp. The C-terminal domain (CTD) contains an Ole e 1-like domain, that was predicted to form beta-sheets that are similar in position and length among Nicotiana spp. and among stylar AGPs. The TTS protein had the greatest amino acid and predicted O-glycosylation conservation among Nicotiana spp. relative to the PELPIII and 120 K. The PELPIII, TTS and 120 K genes undergo negative selection, with d(n)/d(s) ratios of 0.59, 0.29 and 0.38 respectively. The d(n)/d(s) ratio for individual species ranged from 0.4 to 0.9 and from 0.1 to 0.8, for PELPIII and TTS genes, respectively. These data indicate that PELPIII and TTS genes are under different selective pressures. A newly discovered AGP gene, Nicotiana tabacum Proline Rich Protein (NtPRP), was found with a similar intron-exon configuration and protein structure resembling other stylar AGPs, particularly TTS. CONCLUSIONS: Further studies of the NtPRP gene are necessary to elucidate its biological role. Due to its high similarity to the TTS gene, NtPRP may be involved in pollen tube guidance and growth. In contrast to TTS, both PELPIII and 120 K genes are more diverse indicating a possible role in speciation or mating preference of Nicotiana spp. We hypothesize that the stylar AGPs and NtPRP share a common origin from a single gene that duplicated and diversified into four distinct genes involved in pollen-style interactions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1011-2) contains supplementary material, which is available to authorized users.