Multiple evolution of flavonoid 3′,5′-hydroxylase

Abstract

Main conclusion

Multiple F35H evolution from F3H has occurred in dicotyledonous plants. Efficient pollinator attraction is probably the driving force behind, as this allowed for the synthesis of delphinidin-based blue anthocyanins.

The cytochrome P450-dependent monooxygenases flavonoid 3′-hydroxylase (F3′H) and flavonoid 3′,5′-hydroxylase (F3′5′H) hydroxylate the B-ring of flavonoids at the 3′- and 3′- and 5′-position, respectively. Their divergence took place early in plant evolution. While F3′H is ubiquitously present in higher plants, the distribution of F3′5′H is scattered. Here, we report that F3′5′H has repeatedly evolved from F3′H precursors at least four times in dicotyledonous plants: In the Asteraceae, we identified F3′5′Hs specific for the subfamilies Cichorioideae and Asteroideae, and additionally an F3′5′H that seems to be specific for the genus Echinops of the subfamily Carduoideae; moreover, characterisation of a sequence from Billardiera heterophylla (formerly Sollya heterophylla) (Pittosporaceae) showed that the independent evolution of an F3′5′H has occurred at least once also in another family. The evolution of F3′5′H from an F3′H precursor represents a gain of enzymatic function, probably triggered by an amino acid change at one position of substrate recognition site 6. The gain of F3′5′H activity allows for the synthesis of delphinidin-based anthocyanins which usually provide the basis for lilac to blue flower colours. Therefore, the need for an efficient pollinator attraction is probably the driving force behind the multiple F3′5′H evolution.

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Abbreviations

BEBm:

Bayes empirical Bayes

Cy:

Cyanidin

CYP:

Cytochrome P450

Dp:

Delphinidin

GOF:

Gain of function

LOF:

Loss of function

LRT:

Likelihood ratio test

MSA:

Multiple sequence alignment

Pg:

Pelargonidin

SRS:

Substrate recognition site

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Acknowledgments

H. Halbwirth acknowledges funding by the Austrian Science Fund FWF (P24331-B16).

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Correspondence to Heidi Halbwirth.

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Special topic: Polyphenols: biosynthesis and function in plants and ecosystems. Guest editor: Stefan Martens.

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Seitz, C., Ameres, S., Schlangen, K. et al. Multiple evolution of flavonoid 3′,5′-hydroxylase. Planta 242, 561–573 (2015). https://doi.org/10.1007/s00425-015-2293-5

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Keywords

  • Blue flower colour
  • Cytochrome P450-dependent monooxygenase
  • Delphinidin
  • Flavonoid 3′,5′-hydroxylase (F3′5′H)
  • Flavonoid 3′-hydroxylase (F3′H)
  • Pollinator attraction