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Kinetics and functional diversity among the five members of the NADP-malic enzyme family from Zea mays, a C4 species

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Abstract

NADP-malic enzyme (NADP-ME) is involved in different metabolic pathways in several organisms due to the relevant physiological functions of the substrates and products of its reaction. In plants, it is one of the most important proteins that were recruited to fulfil key roles in C4 photosynthesis. Recent advances in genomics allowed the characterization of the complete set of NADP-ME genes from some C3 species, as Arabidopsis thaliana and Oryza sativa; however, the characterization of the complete NADP-ME family from a C4 species has not been performed yet. In this study, while taking advantage of the complete Zea mays genome sequence recently released, the characterization of the whole NADP-ME family is presented. The maize NADP-ME family is composed of five genes, two encoding plastidic NADP-MEs (ZmC4- and ZmnonC4-NADP-ME), and three cytosolic enzymes (Zmcyt1-, Zmcyt2-, and Zmcyt3-NADP-ME). The results presented clearly show that each maize NADP-ME displays particular organ distribution, response to stress stimuli, and differential biochemical properties. Phylogenetic footprinting studies performed with the NADP-MEs from several grasses, indicate that four members of the maize NADP-ME family share conserved transcription factor binding motifs with their orthologs, indicating conserved physiological functions for these genes in monocots. Based on the results obtained in this study, and considering the biochemical plasticity shown by the NADP-ME, it is discussed the relevance of the presence of a multigene family, in which each member encodes an isoform with particular biochemical properties, in the evolution of the C4 NADP-ME, improved to fulfil the requirements for an efficient C4 mechanism.

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Acknowledgments

CSA, MFD and MS are members of the Researcher Career of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) and CEA and EM are fellows of the same institution. We thank Dr. Marcos A. Tronconi for the helpful discussion of sequence analysis. This study has been supported by National Agency for Promotion of Science and Technology (ANPCyT) and CONICET.

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Author notes

  1. Ezequiel Margarit

    Present address: Instituto de Biología Molecular Rosario (IBR) Esmeralda y Ocampo, Edificio IBR-Predio CCT, Rosario, Argentina

Authors and Affiliations

  1. Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI), Universidad Nacional de Rosario, Suipacha 531, Rosario, Argentina

    Clarisa E. Alvarez, Mariana Saigo, Ezequiel Margarit, Carlos S. Andreo & María F. Drincovich

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  1. Clarisa E. Alvarez
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  2. Mariana Saigo
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  3. Ezequiel Margarit
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  4. Carlos S. Andreo
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  5. María F. Drincovich
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Correspondence to María F. Drincovich.

Additional information

Clarisa E. Alvarez and Mariana Saigo contributed equally to this study.

Electronic supplementary material

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11120_2013_9839_MOESM1_ESM.tif

Supplemental Fig. 1 Expression levels of all NADP-ME transcripts in different parts of maize plant Data correspond to the transcript levels in different samples in relation to the expression found for actin1 reference gene. The values obtained are indicated above each bar. The abscissa indicates the samples tested: leaf blades (L); stems (St); roots (R); leaf sheaths (Sh); immature tassels (T); immature ears (E) and 14DAP grains (G). In all the cases, data represent the mean (±SD) of three independent assays (TIFF 186 kb)

Supplemental Table 1 MULAN output of C4-, nonC4-, Cyt1-, and Cyt3- orthologs groups analysis. (XLSX 16 kb)

Supplemental Table 2 Brief descriptions and references of the TF that putatively bind to NADP-ME genes (DOC 53 kb)

11120_2013_9839_MOESM4_ESM.xlsx

Supplemental Table 3 Rice coexpressed transcription factor genes that could putatively bind to the TFBS detected. The genes from O. sativa that share evolutionary conserved TFBS with Z. mays genes were analyzed with RiceFREND web tool. Mutual rank (MR) is the coexpression strength measure. MR = 1 corresponds to the strongest coexpression (XLSX 161 kb)

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Alvarez, C.E., Saigo, M., Margarit, E. et al. Kinetics and functional diversity among the five members of the NADP-malic enzyme family from Zea mays, a C4 species. Photosynth Res 115, 65–80 (2013). https://doi.org/10.1007/s11120-013-9839-9

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  • DOI: https://doi.org/10.1007/s11120-013-9839-9

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