Transcriptional and Morpho-Physiological Responses of Marchantia polymorpha upon Phosphate Starvation

Abstract

Phosphate (Pi) is a pivotal nutrient that constraints plant development and productivity in natural ecosystems. Land colonization by plants, more than 470 million years ago, evolved adaptive mechanisms to conquer Pi-scarce environments. However, little is known about the molecular basis underlying such adaptations at early branches of plant phylogeny. To shed light on how early divergent plants respond to Pi limitation, we analyzed the morpho-physiological and transcriptional dynamics of Marchantia polymorpha upon Pi starvation. Our phylogenomic analysis highlights some gene networks present since the Chlorophytes and others established in the Streptophytes (e.g., PHR1–SPX1 and STOP1–ALMT1, respectively). At the morpho-physiological level, the response is characterized by the induction of phosphatase activity, media acidification, accumulation of auronidins, reduction of internal Pi concentration, and developmental modifications of rhizoids. The transcriptional response involves the induction of MpPHR1, Pi transporters, lipid turnover enzymes, and MpMYB14, which is an essential transcription factor for auronidins biosynthesis. MpSTOP2 up-regulation correlates with expression changes in genes related to organic acid biosynthesis and transport, suggesting a preference for citrate exudation. An analysis of MpPHR1 binding sequences (P1BS) shows an enrichment of this cis regulatory element in differentially expressed genes. Our study unravels the strategies, at diverse levels of organization, exerted by M. polymorpha to cope with low Pi availability.

Tools for In Vitro Propagation/Synchronization of the Liverwort Marchantia polymorpha and Application of a Validated HPLC-ESI-MS-MS Method for Glutathione and Phytochelatin Analysis

“…After additional few days, the pH progressively dropped to a value of 3.5-3.2, and remained constant around this value over the following days (Figure 3). The strong acidification observed in M. polymorpha cultures was also recorded by Rico-Resendiz and colleagues [35] under phosphate starvation conditions, highlighting that acidification can be a mechanism for increasing nutrient availability. Acidification of the medium could be due to the extrusion of metabolites such as organic acids by M. polymorpha gametophytes.…”

An Evolutionarily Conserved Coreceptor Gene Is Essential for CLAVATA Signaling in Marchantia polymorpha

“…Although it is still unclear if the phenotypes in gemma cup formation can be uncoupled from the defects in the apical/subapical cells, MpCLE2 likely regulates cell fates in both the lateral derivatives of the apical cells and the dorsal derivatives of apical/subapical cells. It is known that hormonal and environmental cues affect the formation of gemma cup (Flores-Sandoval et al, 2015;Aki et al, 2019;Li et al, 2020;Rico-Reséndiz et al, 2020). A possible role for MpCLE2 peptide signaling would be to mediate certain environmental cues to control the timing of gemma cup formation and thus clonal propagation, cooperatively with other hormonal inputs.…”

Untargeted In Silico Compound Classification—A Novel Metabolomics Method to Assess the Chemodiversity in Bryophytes

“…The lower chemodiversity of metabolite profiles show that many secondary metabolites degrade due to breakdown. The compound classes of quaternary ammonium salts, amines, and other organonitrogen compounds were enriched in herbarium samples indicating the degradation of amino acids, peptides, and analogues as products of a non-functional respiration metabolism and general catabolic processes [ 70 , 71 , 72 ]. The classes of quaternary ammonium salts are also structurally related to many functional proteins and nitrogen containing glycerophospholipids, which constitute metabolites produced by bryophytes and lichens against desiccation and as a response to reactive oxygen species [ 28 , 73 ].…”