Evolution of nuclear auxin signaling : Lessons from genetic studies with basal land plants

Auxin plays critical roles in growth and development through the regulation of cell differentiation, cell expansion, and pattern formation. The auxin signal is mainly conveyed through a so-called nuclear auxin pathway involving the receptor TIR1/AFB, the transcriptional co-repressor AUX/IAA, and the transcription factor ARF with direct DNA-binding ability. Recent progress in sequence information and molecular genetics in basal plants has provided many insights into the evolutionary origin of the nuclear auxin pathway and its pleiotropic roles in land plant development. In this review, we summarize the latest knowledge of the nuclear auxin pathway gained from studies using basal plants, including charophycean green algae and two major model bryophytes, Marchantia polymorpha and Physcomitrella patens. In addition, we discuss the functional implication of the increase in genetic complexity of the nuclear auxin pathway during land plant evolution

Auxin signaling is essential for organogenesis but not for cell survival in the liverwort Marchantia polymorpha

ゼニゴケを用いて植物ホルモンの役割を証明 --オーキシン信号伝達なくして器官形成なし--. 京都大学プレスリリース. 2023-02-07.Auxin plays pleiotropic roles in plant development via gene regulation upon its perception by the receptors TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX (TIR1/AFBs). This auxin-regulated transcriptional control mechanism originated in the common ancestor of land plants. Although the complete loss of TIR1/AFBs causes embryonic lethality in Arabidopsis thaliana, it is unclear whether the requirement for TIR1-mediated auxin perception in cell viability can be generalized. The model liverwort Marchantia polymorpha has a minimal auxin signaling system with only a single TIR1/AFB, MpTIR1. Here we show by genetic, biochemical, and transcriptomic analyses that MpTIR1 functions as an evolutionarily conserved auxin receptor. Null mutants and conditionally knocked-out mutants of MpTIR1 were viable but incapable of forming any organs and grew as cell masses. Principal component analysis performed using transcriptomes at various developmental stages indicated that MpTIR1 is involved in the developmental transition from spores to organized thalli, during which apical notches containing stem cells are established. In Mptir1 cells, stem cell- and differentiation-related genes were up- and downregulated, respectively. Our findings suggest that, in M. polymorpha, auxin signaling is dispensable for cell division but is essential for three-dimensional patterning of the plant body by establishing pluripotent stem cells for organogenesis, a derived trait of land plants

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RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants

葉緑体が光に集まる反応を制御する新たな因子の発見. 京都大学プレスリリース. 2016-08-30.In green plants, the blue light receptor kinase phototropin mediates various photomovements and developmental responses, such as phototropism, chloroplast photorelocation movements (accumulation and avoidance), stomatal opening, and leaf flattening, which facilitate photosynthesis. In Arabidopsis, two phototropins (phot1 and phot2) redundantly mediate these responses. Two phototropin-interacting proteins, NONPHOTOTROPIC HYPOCOTYL 3 (NPH3) and ROOT PHOTOTROPISM 2 (RPT2), which belong to the NPH3/RPT2-like (NRL) family of BTB (broad complex, tramtrack, and bric à brac) domain proteins, mediate phototropism and leaf flattening. However, the roles of NRL proteins in chloroplast photorelocation movement remain to be determined. Here, we show that another phototropin-interacting NRL protein, NRL PROTEIN FOR CHLOROPLAST MOVEMENT 1 (NCH1), and RPT2 redundantly mediate the chloroplast accumulation response but not the avoidance response. NPH3, RPT2, and NCH1 are not involved in the chloroplast avoidance response or stomatal opening. In the liverwort Marchantia polymorpha, the NCH1 ortholog, MpNCH1, is essential for the chloroplast accumulation response but not the avoidance response, indicating that the regulation of the phototropin-mediated chloroplast accumulation response by RPT2/NCH1 is conserved in land plants. Thus, the NRL protein combination could determine the specificity of diverse phototropin-mediated responses

RSL Class I Genes Controlled the Development of Epidermal Structures in the Common Ancestor of Land Plants

SummaryThe colonization of the land by plants, sometime before 470 million years ago, was accompanied by the evolution tissue systems [1–3]. Specialized structures with diverse functions—from nutrient acquisition to reproduction—derived from single cells in the outermost layer (epidermis) were important sources of morphological innovation at this time [2, 4, 5]. In extant plants, these structures may be unicellular extensions, such as root hairs or rhizoids [6–9], or multicellular structures, such as asexual propagules or secretory hairs (papillae) [10–12]. Here, we show that a ROOTHAIR DEFECTIVE SIX-LIKE (RSL) class I basic helix-loop-helix transcription factor positively regulates the development of the unicellular and multicellular structures that develop from individual cells that expand out of the epidermal plane of the liverwort Marchantia polymorpha; mutants that lack MpRSL1 function do not develop rhizoids, slime papillae, mucilage papillae, or gemmae. Furthermore, we discovered that RSL class I genes are also required for the development of multicellular axillary hairs on the gametophyte of the moss Physcomitrella patens. Because class I RSL proteins also control the development of rhizoids in mosses and root hairs in angiosperms [13, 14], these data demonstrate that the function of RSL class I genes was to control the development of structures derived from single epidermal cells in the common ancestor of the land plants. Class I RSL genes therefore controlled the generation of adaptive morphological diversity as plants colonized the land from the water

Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution.

Chloroplast (cp) DNA is thought to originate from the ancestral endosymbiont genome and is compacted to form nucleoprotein complexes, cp nucleoids. The structure of cp nucleoids is ubiquitously observed in diverse plants from unicellular algae to flowering plants and is believed to be a multifunctional platform for various processes, including cpDNA replication, repair/recombination, transcription, and inheritance. Despite its fundamental functions, the protein composition for cp nucleoids in flowering plants was suggested to be divergent from those of bacteria and algae, but the evolutionary process remains elusive. In this research, we aimed to reveal the evolutionary history of cp nucleoid organization by analyzing the key organisms representing the three evolutionary stages of eukaryotic phototrophs: the chlorophyte alga Chlamydomonas reinhardtii , the charophyte alga Klebsormidium flaccidum , and the most basal land plant Marchantia polymorpha . To clarify the core cp nucleoid proteins in C. reinhardtii , we performed an LC-MS/MS analysis using highly purified cp nucleoid fractions and identified a novel SAP domain-containing protein with a eukaryotic origin as a constitutive core component. Then, homologous genes for cp nucleoid proteins were searched for in C. reinhardtii , K. flaccidum , and M. polymorpha using the genome databases, and their intracellular localizations and DNA binding activities were investigated by cell biological/biochemical analyses. Based on these results, we propose a model that recurrent modification of cp nucleoid organization by eukaryotic factors originally related to chromatin organization might have been the driving force for the diversification of cp nucleoids since the early stage of green plant evolution

Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant

Identification and Biochemical Characterization of the Serine Biosynthetic Enzyme 3-Phosphoglycerate Dehydrogenase in Marchantia polymorpha

L-serine is an important molecule in all living organisms, and thus its biosynthesis is considered to be regulated according to demand. 3-Phosphoglycerate dehydrogenase (PGDH), the first committed enzyme of the phosphorylated pathway of L-serine biosynthesis, is regulated by negative feedback from L-serine in bacteria. In the case of the vascular plant Arabidopsis thaliana, two PGDH isozymes out of three are inhibited by L-serine and activated by L-alanine, L-valine, L-methionine, L-homoserine, and L-homocysteine, suggesting a more complicated regulatory mechanism of L-serine biosynthesis in A. thaliana than in bacteria. However, it remains to be clarified whether the activation mechanism of PGDH by amino acids is conserved in land plants. In this study, we identified the sole isozyme of PGDH in the liverwort Marchantia polymorpha (MpPGDH) and elucidated its biochemical characteristics. MpPGDH cDNA encodes a 65.6 kDa protein that contains a putative transit peptide for chloroplast localization. MpPGDH shares 75–80% identity with A. thaliana isozymes and forms a homotetramer in vitro. Recombinant MpPGDH exhibited an optimal pH of 9.0, apparent Michaelis constants of 0.49 ± 0.04 and 0.096 ± 0.010 mM for 3-PGA and NAD+, respectively, and apparent maximum velocity of 5.65 ± 0.10 μmol⋅min−1⋅mg−1, similar to those of A. thaliana isozymes. Phosphate ions were found to stabilize MpPGDH, suggesting that phosphate ions are also a crucial factor in the regulation of serine biosynthesis via the phosphorylated pathway in Marchantia polymorpha. MpPGDH was inhibited by L-serine in a cooperative manner and was activated by L-alanine, L-valine, L-methionine, L-homoserine, and L-homocysteine to a lesser extent than it is in A. thaliana. The results suggest that an ancestral PGDH of land plants was inhibited byL-serine and slightly activated by five other amino acids