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Tracing Evolution of Auxin Transport and Polarity in Plants

Periodic Reporting for period 4 - ETAP (Tracing Evolution of Auxin Transport and Polarity in Plants)

Periodo di rendicontazione: 2022-07-01 al 2022-12-31

The overall objective of the project is to understand mechanism and evolution of PIN-dependent auxin transport – a versatile and crucial process mediating many developmental events in higher plants, in particular, the plant adaptation to different environmental conditions.

It provided novel insights into how the major multicellular organisms on Earth, the plants, evolved their own specific mechanisms and signalling molecules to regulate their development to cope with challenges of the ever-changing environment.

The project was split into several work packages (WP):

WP1: Establishment of Streptophyta models before colonization of land by plants.
WP2: Origin and early diversification of PIN-dependent auxin transport in plant lineage.
WP3: Source of plant PIN family in prokaryotes: a stepping stone for structural studies.
WP4: Evolution of PIN polarity mechanisms and its endogenous and exogenous regulations.

The project was concluded successfully. We established Klebsorimidium as simple streptophyte model, contributed to establishment of Chara as more complex streptophyte model (WP1). We identified the prototypal PIN auxin transporter from the simple alga Klebsormidium and we showed how the PIN family evolved from this ancestral transporter to become a major regulators of development in land plants (WP2). Despite the prokaryotic PIN homologues were not useful for structural studies, we still contributed to elucidation of structure and function of Arabidopsis PIN1 (WP3). We also provided many novel insights into mechanism of PIN polarity and trafficking mainly in the context of root gravitropism and elucidated mechanism of PIN-mediated canalization (WP4).
To gain insight into evolutionary origins of auxin transport mechanism, we established a morphologically simple multicellular alga Klebsormidium flaccidum as a useful model for early evolutionary studies in plant lineage. We used this model to isolate and characterize the most primitive PIN auxin transporter being functional (Skokan R et al., Nat Plants 2019). We also contributed to the genome sequencing of the morphologically more complex alga Chara braunii (Nishiyama et al., Cell 2018) and identified corresponding PIN sequences. We also provided insights into the complexity of the evolutionary path of PIN proteins by identifying the importance of the intramolecular domain-domain coevolution, which is crucial for their divergent patterns of localization (Zhang Y et al., New Phytologist 2020).

We provided initial and important insights into how plant roots learned to grow down in response to the gravity. We discovered that efficient root gravitropism of higher plants evolved only at the onset of seed plant evolution and was intimately connected to the innovation within PIN proteins that acquired the apical polar localization necessary to efficient gravitropism. This event was an important moment in evolution of plant abilities to colonize efficiently dry land habitats (Zhang Y et al., Nat Commun 2019).
We also discovered critical role of functional innovations within the PIN gene family during evolution as essential prerequisites for the origin of flowering plants and their main parts such as shoot/root, inflorescence, and floral organs (Zhang Y et al., Science Adv 2020).

We also provided key insights into structure of PIN proteins (Abas M et al., PNAS 2021; Yang Z et al., Nature 2022), PIN polarity and trafficking (Glanc M et al., Nat Plants 2018; Glanc et al., Curr Biol. 2021) and into mechanism of auxin canalization (Hajny J et al., Science 2020; Friml J et al., Nature 2022) and auxin signaling for regulation of growth (Fendrych M et al., Nat Plants 2018; Li L et al., Nature 2021; Qi L et al., Nature 2022) and auxin-drived regeneration (Marhava P et al., Cell 2019; Hoermayer L et al., PNAS 2020).
Our studies revealed how during evolution the plant hormone auxin became the major signal regulating growth and forms of plants as we know them today. We specifically provided insights into how the auxin transport function and intricately regulated polar, cellular localization of PIN proteins evolved and how this innovations of PIN protein function and regulation were linked to the increased of morphological complexity and adaptive development of higher plants. The insights into the origin of PIN proteins and identification of the prototypical PIN protein helped elucidate structure of PIN proteins and thus provided the long missing detailed insights into the molecular mechanism of auxin transport. All these results provided an essential ground-work for further understanding of how this unique mechanism of adaptive plant development functioned and how it arose during the progress of the higher plant evolution.
Evolution of polar auxin transporter PIN facilitates the pattern formation of plants
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