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Origin and evolution of auxin-mediated acid growth
Wednesday, 2024/12/25 | 08:26:33

Yue ZengShiyu DengCongcong JinZhiyun ShangLe ChangJiajun WangXue HanAo WangDan Jin,
 Yubo WangHang HeLanxin LiXing Wang Deng deng@pku.edu.cn, and Ning Wei

 

PNAS, December 10 2024; 121 (51) e2412493121; https://doi.org/10.1073/pnas.2412493121

Significance

Although the molecular mechanism underlying acid growth has been basically elucidated in Arabidopsis, its origin and scope in plants remain unclear. Here, we revealed that core genes of acid growth mainly originated in Charophyta and functionally evolved in land plants. However, we found that the PM H+-ATPase in Charophyceae algal Chara braunii is regulated by light instead of auxin, indicating that light control of PM H+-ATPase activity occurred before the regulation by auxin. In addition, we found that auxin elicits transcriptional response and cell elongation independently of canonical auxin receptor TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX (TIR1/AFB) and acid growth in C. braunii. Our study sheds light on how a major growth regulatory pathway such as acid growth might be acquired and developed during plant terrestrialization.

Abstract

The classical acid growth theory suggests that auxin stimulates cell expansion by triggering apoplast acidification via plasma membrane (PM)-localized H+-ATPase. Here, we reconstructed the origin and evolutionary history of auxin-mediated acid growth. Comparative phylogenomic analysis showed that most core components of acid growth originated in Charophyta and then underwent subclass expansion and functional innovation during plant terrestrialization. In Charophyceae algae Chara braunii, we found that PM H+-ATPase has formed a core regulatory module with TMK and PP2C.D, which can be activated by photosynthesis-dependent phosphorylation through light rather than auxin. Despite the lack of canonical auxin receptor TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX (TIR1/AFB), auxin elicits significant internodal elongation and transcriptional reprogramming in C. braunii, implying the existence of an ancient auxin-mediated growth mechanism. We propose that the evolution of acid growth represents a neofunctional adaptation to terrestrial environments, in which PM H+-ATPase in carbon concentrating for photosynthesis was utilized to acidify apoplast for cell expansion, and the core components responsible for acid growth eventually established a regulatory network in land plants by connecting with the TIR1/AFB pathway.

 

See https://www.pnas.org/doi/10.1073/pnas.2412493121

 

Figure 1: Origin and evolution of core components responsible for auxin-mediated acid growth. (A) Identification of the orthologs of core components responsible for acid growth in 30 representative plant species. Circle size represents gene copy number. The ancient whole-genome duplication/triplication events were labeled on the different branches of the phylogenetic tree based on previous reports, and the named duplication events are shown alongside their Greek letter (3839). (B) Gradual coevolution model of auxin-mediated acid growth. The emergence of prominent features across various evolutionary stages is illustrated.

 

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