Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C4 photosynthesis is based on an ancient code found in the ancestral C3 state

Ana Rita Borba, Tânia S. Serra, Alicja Górska, Paulo Gouveia, André M. Cordeiro, Ivan Reyna-Llorens, Jana Kneřová, Pedro M. Barros, Isabel A. Abreu, Maria Margarida Oliveira, Julian M. Hibberd, Nelson J.M. Saibo

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

C4 photosynthesis has evolved repeatedly fromthe ancestral C3 state to generate a carbon concentratingmechanism that increases photosynthetic efficiency. This specialized formof photosynthesis is particularly common in the PACMAD clade of grasses, and is used by many of the world's most productive crops. The C4 cycle is accomplished through cell-typespecific accumulation of enzymes but cis-elements and transcription factors controlling C4 photosynthesis remain largely unknown. Using the NADP-Malic Enzyme (NADP-ME) gene as a model we tested whether mechanisms impacting on transcription in C4 plants evolved from ancestral components found in C3 species. Two basic Helix-Loop-Helix (bHLH) transcription factors, ZmbHLH128 and ZmbHLH129, were shown to bind the C4 NADP-ME promoter from maize. These proteins form heterodimers and ZmbHLH129 impairs trans-activation by ZmbHLH128. Electrophoretic mobility shift assays indicate that a pair of cis-elements separated by a seven base pair spacer synergistically bind either ZmbHLH128 or ZmbHLH129. This pair of cis-elements is found in both C3 and C4 Panicoid grass species of the PACMAD clade. Our analysis is consistent with this cis-element pair originating from a single motif present in the ancestral C3 state. We conclude that C4 photosynthesis has co-opted an ancient C3 regulatory code built on G-box recognition by bHLH to regulate the NADP-ME gene. More broadly, our findings also contribute to the understanding of gene regulatory networks controlling C4 photosynthesis.

Original languageEnglish
Pages (from-to)1690-1705
Number of pages16
JournalMolecular Biology And Evolution
Volume35
Issue number7
DOIs
Publication statusPublished - 1 Jan 2018

Keywords

  • Basic Helix-Loop-Helix
  • C and C photosynthesis
  • Cis-element evolution
  • NADP-Malic Enzyme
  • PACMAD Panicoid grasses

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