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The team led by Deng Xingwang from the College of Modern Agriculture, Peking University, reveals the origin and evolution of the auxin-mediated acidic growth mechanism.
Release time:
2025-03-27
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Publishing Institution: Peking University, School of Modern Agriculture
Journal: PNAS
Impact Factor: 9.4
Publication Date: October 2024
Pronetbio provided yeast signal peptide functional validation services for this study.
In 1971, scientists proposed the famous "acid growth theory" based on the correlation between auxin, cell wall acidification (a process where the pH of the plant cell wall decreases, increasing its extensibility), and cell elongation.
The classical acid growth theory suggests that auxin promotes H+ efflux by stimulating proton pumps (PM H+-ATPase) on the plant cell membrane, leading to cell wall acidification and activation of cell wall remodeling proteins such as expansins (EXP), which in turn facilitates water uptake, cell expansion, and elongation.
While the auxin-regulated phosphorylation pathway of proton pumps has been well studied, some research indicates that auxin receptors TIR1/AFB are only found in terrestrial plants. Thus, the origin and evolution of the auxin-mediated acid growth regulatory network remain an unresolved question.
In October 2024, a research paper titled "Origin and Evolution of Auxin-mediated Acid Growth"was published online in PNAS by a team led by Xingwang Deng from the School of Modern Agriculture, Peking University. Haiyue Zeng was the first author, while Academician Xingwang Deng from Peking University and Professor Ning Wei from Southwest University served as corresponding authors. Through comparative genomic and phylogenetic analyses across plant lineages, as well as experimental validation in key species, the study proposed a progressive evolutionary model for the acid growth mechanism and auxin system.
Research Content
The researchers conducted comparative genomic and phylogenetic analyses on the core components of the acid growth pathway, including PM H+-ATPase (proton pump on the plasma membrane), PP2C.D (phosphatase), TMK (transmembrane kinase), SAUR (auxin rapid response gene and PP2C.D inhibitor), EXP (cell wall remodeling protein), and ABP1/ABL (auxin-binding protein). They found that these genes are present in Chara braunii (a species of Charophyte algae). Based on detailed analyses of these core genes and related experiments, the study uncovered the following key findings:
1. Functional Differences in Proton Pumps Between Chara braunii and Terrestrial Plants
The study found that PM H+-ATPase is conserved across plant lineages. RT-qPCR results showed that CbHA2 (a PM H+-ATPase isoform) is the dominant form in Chara braunii, and its transmembrane helix structure differs from that of most land plants. Furthermore, experiments revealed that the phosphorylation of C. braunii proton pumps is activated by light signals rather than by auxin, suggesting functional differences between the proton pumps of C. braunii and those of terrestrial plants.
Additionally, analysis of core genes regulating PM H+-ATPase (PP2C.D, TMK, SAUR, EXP, and ABP1/ABL) revealed that these genes first appeared during the Charophyte stage.
2. Homologous Proteins of PP2C.D and TMK in Chara braunii Can Interact with Proton Pumps
Homologous proteins of TMK and PP2C.D were identified in C. braunii. Membrane-based yeast two-hybrid and co-immunoprecipitation (Co-IP) experiments demonstrated that they might form an interaction module with CbHA2, resembling the PM H+-ATPase-TMK/PP2C.D module found in terrestrial plants.
3. The Origin, Expansion, and Functional Evolution of the SAUR Gene Family
Yeast two-hybrid assays showed that SAUR in C. braunii cannot directly regulate PP2C.D. Further studies revealed that C. braunii SAUR primarily responds to ethylene. Researchers hypothesize that through multiple gene duplication events, certain C-SAURs in vascular plants underwent functional diversification, acquiring the ability to interact with PP2C.D and eventually becoming a crucial component of acid growth.
4. Functional Evolution of the EXP Superfamily During the Zygnematophyceae Stage
Phylogenetic analysis suggested that green algal EXPs may represent the ancestral form of the EXP family. Further analysis revealed that during the Zygnematophyceae stage, EXP genes underwent extensive duplication and acquired new functions. This shift played a key role in the transition of EXP function toward acid-induced regulation during land plant evolution.
Figure 1: The core regulatory genes of acid growth primarily originated in Charophytes and fully emerged in terrestrial plants. Chara braunii possesses all the core genes required for acid growth.
5. In Certain Plant Species, ABP1/ABL Is Absent, and Its Function Is Performed by Unknown Cupin Proteins
ABP1 is found in algae, land plants, and bacteria, while ABL is detected only in seed plants. These proteins bind auxin and form a core receptor complex with TMK, which phosphorylates PM H+-ATPase at pT, thereby activating acid growth.
Yeast signal peptide assays confirmed that the signal peptides of KnABP1 (Klebsiella oxytoca) and AtABP1 (Arabidopsis thaliana) are essential for protein secretion.
Since ABP1 has low auxin-binding affinity in the high-pH cytoplasmic environment, auxin cannot efficiently bind to ABP1 within the cytoplasm. Thus, signal peptide-mediated extracellular localization may be essential for ABP1’s auxin-binding capability.
In certain species where ABP1/ABL is absent and the signal peptide responsible for protein secretion is missing, the function of auxin binding, which is typically carried out by ABP1/ABL, might be performed by unknown cupin proteins.
Figure 2: Evaluation of ABP1 Signal Peptide Secretion Function in the Yeast System
Summary
1. The origin and evolution of the auxin-mediated acid growth mechanism is a gradual process.
2. The core regulatory genes of acid growth were already present in Charophytes, but at that stage, the proton pump functioned as part of the light signaling pathway and was not yet responsive to auxin. Instead, cell expansion in algae was regulated by an unknown auxin-related system.
3. Signal peptide-mediated protein secretion may be essential for ABP1 to bind auxin.
4. During the transition of plants from water to land, several key evolutionary changes occurred: the emergence of TIR1/AFB receptors, gene duplication leading to the neofunctionalization of acid growth-related genes, and innovations in plant cell wall composition. These changes allowed auxin signaling to replace light signaling as the primary regulatory signal for proton pumps, making auxin the key driver of acid growth regulation in terrestrial plants.
Figure 3: Gradual Evolutionary Model of the Auxin-Mediated Acid Growth Mechanism
Project Introduction
This study acknowledges Nanjing Pronet Biotech for providing yeast signal peptide screening technology services.
Technical Advantages:
1. Easy Observation: The signal peptide secretion function can be visually observed through a colorimetric reaction.
2. Stable and Efficient: The yeast signal peptide functional verification system has been widely applied in biological research.
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