Functional PTB phosphate transporters are present in streptophyte algae and early diverging land plants

Abstract

SummaryTwo inorganic phosphate (Pi) uptake mechanisms operate in streptophytes and chlorophytes, the two lineages of green plants. PHOSPHATE TRANSPORTER B (PTB) proteins are hypothesized to be the Na + /Pi symporters catalysing Pi uptake in chlorophytes, whereas PHOSPHATE TRANSPORTER 1 (PHT1) proteins are the H + /Pi symporters that carry out Pi uptake in angiosperms. PHT1 proteins are present in all streptophyte lineages. However, Pi uptake in streptophyte algae and marine angiosperms requires Na + influx, suggesting that Na + /Pi symporters also function in some streptophytes. We tested the hypothesis that Na + /Pi symporters exist in streptophytes. We identified PTB sequences in streptophyte genomes. Core PTB proteins are present at the plasma membrane of the liverwort Marchantia polymorpha. The expression of M. polymorpha core PTB proteins in the Saccharomyces cerevisiae pho2 mutant defective in high-affinity Pi transport rescues growth in low-Pi environments. Moreover, levels of core PTB mRNAs of M. polymorpha and the streptophyte alga Coleochaete nitellarum are higher in low-Pi than in Pi-replete conditions, consistent with a role in Pi uptake from the environment.We conclude that land plants inherited two Pi uptake mechanisms -mediated by the PTB and PHT1 proteins, respectively -from their streptophyte algal ancestor. Both systems operate in parallel in extant early diverging land plants.

Neofunctionalisation of basic helix−loop−helix proteins occurred when embryophytes colonised the land

“…We further searched the C. braunii genome and transcriptome assemblies (Nishiyama et al ., ) using the same queries and the complete sequence of the putative C. braunii class VIII bHLH protein as a query, but did not identify further new class VIII sequences. Using the same method, we identified a single full‐length nucleotide sequence encoding a putative class VIII bHLH protein of 574 amino acid from a Coleochaete nitellarum transcriptome (Bonnot et al ., ) (Dataset S1). No putative class VIII bHLH sequence was found in the genome of Klebsormidium nitens (Hori et al ., ; Catarino et al ., ).…”

“…These axes develop a diversity of cell types including tip‐growing cells called rhizoids that are involved in nutrient uptake (Box, , ; Andrews, ; Vermeer et al ., ; Wüestenberg et al ., ) and anchorage (Graham & Wilcox, ). Tip‐growing cells involved in nutrient uptake and anchorage also evolved among the land plants (Jones & Dolan, ; Bonnot et al ., ): the tip‐growing rhizoids of bryophytes and root hairs of vascular plants. No other streptophyte algae form morphogenetic centres or develop the same level of cellular complexity that is characteristic of the charophycean algae (Pickett‐Heaps, ; Graham & Wilcox, ).…”

“…To identify class VIII sequences in Chara braunii and Coleochaete nitellarum , we used the land plants bHLH class VIII protein sequences of Arabidopsis thaliana , Selaginella moellendorffii , Physcomitrella patens and Marchantia polymorpha published previously (Catarino et al ., ) as queries in T Blast N searches (Altschul et al ., ) of the C. braunii genome (Nishiyama et al ., ) and transcriptome (as detailed in the ‘Construction of the C. braunii transcriptome’ subsection) and of the Coleochaete nitellarum transcriptome (Bonnot et al ., ). We also searched for bHLH class VIII sequences in the transcriptomes of other streptophyte algae available in the OneKP database (Matasci et al ., ).…”

Neofunctionalisation of basic helix loop helix proteins occurred when plants colonised the land

“…We further searched the C. braunii genome and transcriptome assemblies (Nishiyama et al , 2018), using the same queries and the complete sequence of the putative C. braunii class VIII bHLH protein as a query but did not identify further new class VIII sequences. We also identified a putative class VIII bHLH protein from a Coleochaete nitellarum transcriptome (Bonnot et al , 2017) (Supplementary Data 1). No putative class VIII bHLH sequence was found in Klebsormidium flaccidum (Hori et al , 2014; Catarino et al , 2016).…”

“…To identify class VIII sequences in Chara braunii and Coleochaete nitellarum , we used the and plants bHLH class VIII protein sequences of Arabidopsis thaliana , Selaginella moelendorfii , Physcomitrella patens and Marchantia polymorpha published previously (Catarino et al , 2016) as queries in TBlastN searches (Altschul et al , 1990) of Coleochaete nitellarum transcriptome (Bonnot et al , 2017) and C. braunii genome (Nishiyama et al , 2018) and transcriptome (see “Construction of the C. braunii transcriptome” hereafter). No E-value thresholds were used.…”