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From dimer to tetramer: the evolutionary trajectory of C4 photosynthetic-NADP-ME oligomeric state in Poaceae

ABSTRACT: In maize, two plastidic NADP-malic enzyme (C4-NADP-ME) isoforms are present: C4-NADP-ME and nonC4-NADP-ME, each with distinct kinetic and structural features. To investigate the differences in oligomeric states of C4- and nonC4-NADP-ME in plant tissues, we analyzed extracts of maize from etiolated leaves and roots using native PAGE coupled with an in-gel NADP-ME activity assay. All protein bands exhibiting NADP-ME activity were excised and analyzed by mass spectrometry.

INSTRUMENT(S):

ORGANISM(S): Zea Mays (maize)

TISSUE(S): Root, Leaf

SUBMITTER: Gereon Poschmann

LAB HEAD: Gereon Poschmann

PROVIDER: PXD059557 | Pride | 2026-05-25

REPOSITORIES: Pride

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Dataset's files

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			Action	DRS
	20231019_Zea_mays_ME_2entries_GP.fasta	Fasta
	LM08085.msf	Msf
	LM08085.pdResult	Other
	LM08085.raw	Raw
	LM08086.msf	Msf

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Publications

A milestone in C4 carbon concentration mechanism evolution: structural remodeling of NADP-malic enzyme in Poaceae.

Böhm Jonas M JM Willms Simone S Ferrao Oja O Buitrago-Arango Martin M Hüdig Meike M Poschmann Gereon G Fazelnia Nazanin N Nagel-Steger Luitgard L Klinke Sebastián S Drakonaki Athina A Gatsogiannis Christos C Tronconi Marcos A MA Alvarez Clarisa E CE Maurino Veronica G VG

Molecular biology and evolution 20260401 4

The evolution of C4 photosynthesis required extensive modification of ancestral enzymes enabling the development of an efficient carbon concentrating mechanism. A key example is NADP-malic enzyme (NADP-ME), which, in maize and sorghum-members of the same C4 lineage-underwent gene duplication and neofunctionalization, resulting in 2 plastidic isoforms with distinct oligomeric states: a tetrameric C4-specific isoform and a dimeric housekeeping (nonC4) isoform. In this study, we resolve the structu ...[more]

PMID: 42017302

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Comparative histone modification profiling revealed developmentally regulated acetylation on upstream promoters of C4 genes and potential C4 regulators

Project description:We analysed genome-wide histone H3 lysine 4 trimethylation and histone H3 lysine 9 acetylation, two modifications typically associated with active genes, in meristematic cells at the base and expanding cells in the maturing zone of the maize (Zea mays) leaf. These data were compared to transcript levels of associated genes. Our data revealed that for individual genes fold-changes in histone modification and transcript abundance were much better correlated than absolute intensities. When focusing on regulated modification sites, we identified secondary upstream H3 lysine 9 acetylation peaks (SUPs) on upstream promoter regions of approximately 6% of all acetylated genes. SUPs showed stronger regulation than the previously described acetylation peaks at transcription initiation sites, were more often found on genes that were upregulated towards the maturing zone than on downregulated genes, and were significantly enriched on photosynthetic genes. We identified SUPs on all genes encoding enzymes of the C4 cycle. Moreover, SUPs were enriched in four lists of candidate C4-associated genes that were derived from previous transcriptomic studies. Based on these data, we used highly regulated SUPs as an epigenetic mark to identify new genes potentially involved in C4 metabolism. This approach also allowed the identification of ethylene response elements as highly enriched cis-acting elements in SUP regions. Our data suggest co-evolution of epigenetic promoter elements during the establishment of C4 photosynthesis. Comparative analysis of H3K9ac, H3K4me3 and the transcription between two developmental zones within one maize leaf.

2015-09-03 | E-GEOD-67551 | biostudies-arrayexpress

Respiratory and C4-photosynthetic NAD-malic enzyme coexist in bundle sheath cells mitochondria and evolved via association of differentially adapted subunits

Project description:In Cleomaceae species, NAD-malic enzyme (NAD-ME) was independently co-opted to participate in C4 photosynthesis. In C4 Cleome species, all NAD-ME genes (NAD-MEα, -ß1 and -ß2) were affected by C4 evolution and are expressed at higher levels than their C3 orthologs in Tarenaya hassleriana. In C3 Cleome, the NAD-ME housekeeping function is performed by two heteromers, NAD-MEα/ß1 and NAD-MEα/ß2, with similar biochemical properties and tissue occurrence. In the C4 species, Gynandropsis gynandra and Cleome angustifolia, this role is performed only by the NAD-MEα/ß2 heteromer. In these C4 species NAD-MEα/ß1 is preferentially present in leaves of the C4 species where is the predominant isoform. GgNAD-MEα/ß1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate. In C4 Cleome NAD-MEα/ß1 represents thus the C4-decarboxylase. GgNAD-MEß1and CaNAD-MEß1 are non-catalytic subunits but impart a stabilizing effect on the associated α-subunit. We conclude that in C4 Cleome the functions of NAD-ME as a TCA cycle associated enzyme and as a C4 photosynthetic decarboxylase coexist in BSC mitochondria and are performed by isoforms originated through associations of differentially adapted subunits.

2021-11-30 | PXD026547 | Pride

Exploring the mechanism of C4 photosynthetic differentiation through a unified comparative analysis of maize and rice leaf transcriptomes

Project description:Maize and rice are the two most economically important grass crops and utilize distinct forms of photosynthesis to fix carbon: C4 and C3 respectively. Relative to C3 photosynthesis, C4 photosynthesis reduces photorespiration and affords higher water and nitrogen use efficiencies under hot arid conditions. To define key innovations in C4 photosynthesis, we profiled metabolites and gene expression along a developing leaf gradient. A novel statistical method was implemented to compare transcriptomes from these two species along a unified leaf developmental gradient and define candidate cis-regulatory elements and transcription factors driving photosynthetic gene expression. We also present comparative primary and secondary metabolic profiles along the gradients that provide new insight into nitrogen and carbon metabolism in C3 and C4 grasses. These resources, including community viewers to access and mine these datasets, will enable the elucidation and engineering of C4 photosynthetic networks to improve the photosynthetic capacity of C3 and C4 grasses. [Maize] Nine day old third leaves of maize were cut into fifteen 1 cm segments; samples were pooled from an average of seven plants per biological replicate and six biological replicates in total were collected on different dates. [Rice] 14 day old third leaves of rice were cut into eleven 2 cm segments, samples were pooled from an average of 15 plants per biological replicate and four replicates in total were collected.

2014-10-12 | E-GEOD-54274 | biostudies-arrayexpress

Exploring the mechanism of C4 photosynthetic differentiation through a unified comparative analysis of maize and rice leaf transcriptomes

2014-10-12 | GSE54274 | GEO

Comparative histone modification profiling revealed developmentally regulated acetylation on upstream promoters of C4 genes and potential C4 regulators

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Structural and Metabolic Transitions of C4 Leaf Development and Differentiation Defined by Microscopy and Quantitative Proteomics in Maize

Project description:C4 grasses, such as maize (Zea mays), have high photosynthetic efficiency through combined biochemical and structural adaptations.C4 photosynthesis is established along the developmental axis of the leafblade, leading from an undifferentiated leaf base just above the ligule into highly specialized mesophyll cells (MCs) and bundle sheath cells (BSCs) at the tip. To resolve the kinetics of maize leaf development and C4 differentiation and to obtain a systems-level understanding of maize leaf formation, the accumulation profiles of proteomes of the leaf and the isolated BSCs with their vascular bundle along the developmental gradient were determined using large-scale mass spectrometry. This was complemented by extensive qualitative and quantitative microscopy analysis of structural features (e.g., Kranz anatomy, plasmodesmata, cell wall, and organelles). More than 4300 proteins were identified and functionally annotated. Developmental protein accumulation profiles and hierarchical cluster analysis then determined the kinetics of organelle biogenesis, formation of cellular structures, metabolism, and coexpression patterns. Two main expression clusters were observed, each divided in subclusters, suggesting that a limited number of developmental regulatory networks organize concerted protein accumulation along the leaf gradient. The coexpression with BSC and MC markers provided strong candidates for further analysis of C4 specialization, in particular transporters and biogenesis factors. Based on the integrated information, we describe five developmental transitions that provide a conceptual and practical template for further analysis. An online protein expression viewer is provided through the PlantProteomeDatabase.

2023-10-12 | PXD046098 | Pride

Developmental Dynamics of Kranz Cell Transcriptional Specificity in Maize Leaf Reveals Early Onset of C4-related Processes

Project description:The comparison of the cell-specific transcriptomes of bundle sheath (BS) and mesophyll (M) cells from successive developmental stages of maize leafs reveals that the number of genes preferentially transcribed in one cell type or the other varies considerably from the sink-source transition to mature photosynthetic stages. The number of differentially expressed (DE) genes is maximal at a stage well prior to full maturity, including those that encode key functions for C4 photosynthesis. The developmental dynamics of BS/M differential expression can be used to identify candidates for other C4-related functions and to simplify the identification of specific pathways members from otherwise complex gene families. The candidates for C4-related transcription factors identified with this developmental DE strategy overlap with those identified in studies using alternative strategies. Nine day old third leaves of maize sections, located at -1 cm, +4 cm and +9 cm (leaf tip), relative to the sink-source transition, were collected. BS and M cells were captured from each section. There are two duplications for each section and each cell types. A total of 12 libraries were constructed for RNA-seq.

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Gene expression profile of liver obtained from liver-specific Me1-deficient mice challenged with high-fat diet

Project description:Nonalcoholic fatty liver disease (NAFLD) has grown from a relatively unknown disease to the leading chronic liver disease globally. Malic enzyme 1 (ME1) is a cytosolic NADP+-dependent enzyme involved in the oxidative decarboxylation of malate to pyruvate while concomitantly generating nicotinamide adenine dinucleotide phosphate (NADPH) from NADP+. Previous genome-wide association studies have identified ME1 as a susceptibility gene for obesity and diabetes. This analysis was performed to understand the transcriptomic changes associated with hepatic Me1 loss in male mice challenged with high-fat diet.

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