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Citrulline metabolism in plants

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Abstract

Citrulline was chemically isolated more than 100 years ago and is ubiquitous in animals, plants, bacteria, and fungi. Most of the research on plant citrulline metabolism and transport has been carried out in Arabidopsis thaliana and the Cucurbitaceae family, particularly in watermelon which accumulates this non-proteinogenic amino acid to very high levels. Industrially, citrulline is produced via specially optimized microbial strains; however, the amounts present in watermelon render it an economically viable source providing that other high-value compounds can be co-extracted. In this review, we provide an overview of our current understanding of citrulline biosynthesis, transport, and catabolism in plants additionally pointing out significant gaps in our knowledge which need to be closed by future experimentation. This includes the identification of further potential enzymes of citrulline metabolism as well as obtaining a far better spatial resolution of both sub-cellular and long-distance partitioning of citrulline. We further discuss what is known concerning the biological function of citrulline in plants paying particular attention to the proposed roles in scavenging of excess NH4 + and as a compatible solute.

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Authors and Affiliations

  1. Texas A&M AgriLife Research and Extension Center, Texas A&M University, Uvalde, TX, 78801, USA

    Vijay Joshi

  2. Max-Planck-Institute for Molecular Plant Physiology, Wissenschaftspark Golm, 14476, Potsdam-Golm, Germany

    Alisdair R. Fernie

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  1. Vijay Joshi
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Correspondence to Vijay Joshi.

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Handling Editor: J. D. Wade.

Electronic supplementary material

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726_2017_2468_MOESM1_ESM.pdf

Supplementary material 1 (PDF 783 kb) Supplemental Table 1 Table shows gene IDs associated with citrulline metabolism in watermelon and orthologous genes from selected Cucurbita species retrieved from the website of the Cucurbit Genomics Database (International Cucurbit Genomics Initiative; ICuGI; http://cucurbitgenomics.org/)

Supplementary material 2 (PDF 110 kb)

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Supplementary material 3 (PDF 296 kb) Supplemental Fig. 1 Percent distribution of total amino acids across the rind and flesh tissues in the matured watermelon fruit (cultivar; Charleston Gray; n = 4).

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Supplementary material 4 (PDF 403 kb) Supplemental Fig. 2 Alignment of watermelon OTC (Cla020781) with OTCases from XP_008466541 (Cucumis melo), XP_004147858 (Cucumis sativus), XP_007223218 (Prunus persica), NP_001316345 (Solanum lycopersicum), XP_007136615 (Phaseolus vulgaris), NP_177667 (Arabidopsis thaliana), XP_015625132 (Oryza sativa Japonica), AAI07155.1 (Homo sapiens), and WP_021561032 (Escherichia coli). The conserved SMRTR (residues 126–130) carbamoyl-P binding domain and the FMHCLP (residues 333–338) a binding domain for l-ornithine are highlighted in purple. Protein alignments were carried out using the Clustal Omega program (McWilliam et al. 2013)

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Supplementary material 5 (PDF 516 kb) Supplemental Fig. 3 Alignment of watermelon N-acetylornithine deacetylase NAODs (Cla016179, Cla016181, Cla016180—DIP1) with AODs from AAG25896.1 (Cucurbita pepo), XP_008465960.1, XP_008465958.1, XP_008465959.1 (Cucumis melo), Q9C5C4 (At4g17830—Arabidopsis thaliana), NP_418392.1 (Escherichia coli), and Csa3G902920, Csa3G902910, and Csa3G902410 (Cucumis sativus). Protein alignments were carried out using the Clustal Omega program (McWilliam et al. 2013)

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Supplementary material 6 (PDF 455 kb) Supplemental Fig. 4 Alignment of watermelon arginosuccinate synthase/synthetase ASSs (Cla019267, Cla002611, Cla002609) with ASSs from AT4G24830 (Arabidopsis thaliana), LOC_Os12g13320.1 and LOC_Os11g19770.1 (Oryza sativa Japonica), XP_004138056.1 (Cucumis sativus), ACI77470 (Escherichia coli), and AAA51783 (Homo sapiens). The conserved region (S-x-D-x-N-x(6)-E) involved in the citrulline and ATP binding, domain (E-[N/D]-R-x(4)-K-x(4)-Y-E) involved in the citrulline–aspartate binding loop and the consensus sequence (G-x-T-x-K-G-N-D-x(2)-R-F) involved in the aspartate binding are shown in green colors. Protein alignments were carried out using the Clustal Omega program (McWilliam et al. 2013)

726_2017_2468_MOESM7_ESM.pdf

Supplementary material 7 (PDF 425 kb) Supplemental Fig. 5 Alignment of watermelon arginosuccinate lyase ASLs (Cla022154, Cla023055) with ASLs from AT5G10920 (Arabidopsis thaliana), LOC_Os03g19280.1 (Oryza sativa Japonica), WP_032252793.1 (Escherichia coli), XP_008466162 (Cucumis melo), XP_004136255 (Cucumis sativus) and pdb|1AOS (Homo sapiens). The conserved region DREDV region shows arginine ‘R’ residue that led to the point mutation red1 (R140L) in the rice argininosuccinate lyase (ASL). Protein alignments were carried out using the Clustal Omega program (McWilliam et al. 2013)

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Supplementary material 8 (PDF 169 kb) Supplemental Fig. 6 Phylogenetic analysis of putative amino acid transporters from watermelon and Arabidopsis generated using multiple sequence alignment using Clustal Omega program (Sievers et al. 2011)

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Supplementary material 9 (PDF 24 kb) Supplemental Fig. 7a and 7b Phylogenetic tree of selected amino acid permeases and sequence alignment of selected watermelon (Cla023090, Cla013912, Cla023187) genes with RcAAP3 (NP_001310657.1 amino acid permease 3; Ricinus communis), AtAAP3 (NP_177862.1 amino acid permease 3; Arabidopsis thaliana), AtAAP5 (NP_175076.2 amino acid permease 5; Arabidopsis thaliana), OsAAP1 (BAG99938.1 Oryza sativa Japonica), OsAAP3 (BAG95706.1 Oryza sativa Japonica), AtAAP1 (NP_176132.1; Arabidopsis thaliana) and AtAAP58 (NP_172472.1; Arabidopsis thaliana)

Supplementary material 10 (PDF 418 kb)

726_2017_2468_MOESM11_ESM.pdf

Supplementary material 11 (PDF 302 kb) Supplemental Fig. 8 Prediction of transmembrane helices in the watermelon genes (Cla023090, Cla013912, Cla023187) was calculated using TMHMM (Krogh et al. 2001). The description of analysis shows a number of predicted TMHs—predicted the number of transmembrane helices, expected the number of amino acids in transmembrane helices, expected number of amino acids in transmembrane helices in the first 60 amino acids of the protein

Supplementary material 12 (PDF 230 kb)

Supplementary material 13 (PDF 229 kb)

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Joshi, V., Fernie, A.R. Citrulline metabolism in plants. Amino Acids 49, 1543–1559 (2017). https://doi.org/10.1007/s00726-017-2468-4

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