[荷爾蒙與演化] 藻類是生長素反應的起源？ 20191003 PLoS genetics

Evolution of the Auxin Response Factors from charophyte ancestors

Raquel Martin-Arevalillo,Emmanuel Thévenon,Fanny Jégu,Thomas Vinos-Poyo,Teva Vernoux,François Parcy,Renaud Dumas

Abstract

Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most ‘ancient’ ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares many features with modern ARFs: it is capable of oligomerization, interacts with the TOPLESS co-repressor and specifically binds Auxin Response Elements as dimer. In addition, CaARF possesses a DNA-binding specificity that differs from class A and B ARFs and that was maintained in class C ARF along plants evolution. Phylogenetic evidence together with CaARF biochemical properties indicate that the different classes of ARFs likely arose from an ancestral proto-ARF protein with class C-like features. The foundation of auxin signalling would have thus happened from a pre-existing hormone-independent transcriptional regulation together with the emergence of a functional hormone perception complex.

Author summary

Plants transition from water to land was determining for the history of our planet, since it led to atmospheric and soil condition changes that promoted the appearance of other life forms. This transition initiated around 1 billion years ago from a Charophyte algae lineage that acquired features allowing it to adapt to the very different terrestrial conditions. Land plants coordinate their development with external stimuli through signalling mechanisms triggered by plant hormones. Therefore, evolution of these molecules and their signalling pathways likely played an important role in the aquatic to terrestrial move. In this manuscript we study the origin of auxin signalling, a plant hormone implicated in all plant developmental steps. Our studies suggest that out of the three families of proteins originally proposed to trigger auxin signalling in land plants, only one existed in Charophyte ancestors as a likely transcriptional repressor independent of auxin. We show that despite millions of years of evolution, this family of proteins has conserved its biochemical and structural properties that are found today in land plants. The results presented here provide an insight on how hormone signalling pathways could have evolved by co-opting a pre-existing hormone-independent transcriptional regulatory mechanism.

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從輪藻來看生長素轉錄因子的演化

摘要

生長素是在植物中一個主要的生長調節物質。在演化上獲得對於生長素產生轉錄反應的事件，很可能令植物產生了發育上的創新。而這件事的發生也許和植物從水生進一步演進成陸生，在相同的時期產生。在陸生植物中，生長素反應轉錄因子（ARFs）所媒介的生長素基因轉錄反應，可被分為A、B及C三個演化種類。而在藻類中，ARF的起源與本質仍然有諸多討論。在此，我們從演化早期分枝出的輪藻（Chlorokybus atmophyticus）中，辨識出了到目前為止最“古老”的ARF相似基因，CaARF。以結構模擬再加上生物化學的研究顯示，CaARF與現代的ARF們，共同享有許多相似的特性：可以形成多聚體，能夠與共同抑制蛋白TOPLESS互動以及可以以二聚體的型態，與生長素反應片段（去氧核醣核酸片段）有針對性的結合。此外，CaARF具有與A、B兩類不同的去氧核醣核酸親和力，這個特性則在演化中，在C類的ARF中被保存了下來。演化學的證據再加上CaARF的生化特性，顯示出不同類型的ARF可能是從具有C類特性的原始ARF所衍生出來。因此，生長素的訊息傳導的基礎，可能是由一個原來就存在的，與荷爾蒙無關的轉錄機制，再加上一個功能性的荷爾蒙接收複合體所建構而成。

作者總結

植物從水中轉移到陸地是地球歷史上的轉淚點，這個事件導致了大氣與土壤的環境改變，也促進了其他物種的衍生。這個轉變發生在大約一億年前，從輪藻類綠藻獲得了特定的特性，而能適應非常不同的陸地生活型態開始。陸生植物針對外界的刺激，會經由植物荷爾蒙誘發的訊息傳導機制，來調整他們的生長發育。因此，這些荷爾蒙分子與他們的訊息傳遞途徑，很可能在水生轉移到陸生的過程中，扮演了很重要的角色。在這篇研究中，我們探討了生長素（在幾乎所有植物生長發育時期都有重要功能的植物荷爾蒙）訊息的緣起。我們的研究暗示了，在植物中，三個被推測調節生長素反應的蛋白質家族裡，只有一類有類似的祖先蛋白存在於輪藻中，並且可能參與了與生長素無關的轉錄抑制功能。我們展示了，雖然經過了數百萬年的演化，這群蛋白質與現今植物中，所存在的蛋白植有極相似的生化與結構特性。這些結果在了荷爾蒙訊息傳導的演化上，如何經由調整已經存在、且獨立於荷爾蒙反應的轉錄機制，逐漸演化出來的途徑，提供了一條線索。