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Parallel pigment and transcriptomic analysis of four barley Albina and Xantha mutants reveals the complex network of the chloroplast-dependent metabolism

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Abstract

We investigated the pigment composition and the transcriptome of albina (alb-e 16 and alb-f 17) and xantha (xan-s 46 and xan-b 12) barley mutants to provide an overall transcriptional picture of genes whose expression is interconnected with chloroplast activities and to search for candidate genes associated with the mutations. Beside those encoding plastid-localized proteins, more than 3,000 genes involved in non-chloroplast localized metabolism were up-/down-regulated in the mutants revealing the network of chloroplast-dependent metabolic pathways. The alb-e 16 mutant was characterized by overaccumulation of protoporphyrin IX upon ALA (5-amino levulinic acid) feeding and down-regulation of the gene encoding one subunit of Mg-chelatase, suggesting a block of the chlorophyll biosynthetic pathway before Mg-protoporphyrin IX biosynthesis, while alb-f 17 overaccumulated Mg-protoporphyrin IX and repressed PorA expression, without alterations in Mg-chelatase mRNA level. The alb-f 17mutant also showed overexpression of several genes involved in phytochrome and in phytochrome-dependent pathways. The results indicate that the down-regulation of Lhcb genes in alb-e 16 cannot be mediated by the accumulation of Mg-protoporphyrin IX. After ALA treatment, xan-s 46 showed overaccumulation of Mg-protoporphyrin IX, while the relative porphyrin composition of xan-b 12 was similar to wild type. The transcripts encoding the components of several mitochondrial metabolic pathways were up-regulated in albina/xantha leaves to compensate for the absence of active chloroplasts. The mRNAs encoding gun3, gun4, and gun5 barley homologous genes showed significant expression variations and were used to search for co-expressed genes across all samples. These analyses provide additional evidences on a chloroplast-dependent covariation of large sets of nuclear genes.

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Abbreviations

ABA:

Abscisic acid

ALA:

5-Amino levulinic acid

CAO:

Chlorophyll a oxigenase

Chlide:

Chlorophyllide

DVPchlide:

Divinylprotochlorophyllide

GluTR:

Glutamyl-tRNA-reductase

GO:

Gene ontology

Gun :

Genome uncoupled

Mg-proto IX:

Mg-protoporphyrin IX

Mg-proto MME:

Mg-protoporphyrin-monomethylester

MMC:

Mg-proto IX MME cyclase

MCCase:

Methylcrotonyl-CoA carboxylase

MVPchlide:

Monovinylprotochlorophyllide

Pchlide:

Protochlorophyllide

POR:

Protochlorophyllide-oxidoreductase

Proto IX:

Protoporphyrin IX

PS:

Photosystem

qRT-PCR:

Quantitative reverse transcription-PCR

VDE:

Violaxanthin de-epoxidase

WT:

Wild type

ZEP:

Zeaxanthin epoxidase

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Acknowledgments

This work was supported by the FIRB programs No. RBAU01E3CX and No. RBIP06CTBR (Parallelomics). We thank Prof. Timothy J. Close (University of California, Riverside, CA) for his help in array analysis, Prof. Diter von Wettstein (Washington State University, Pullman, WA) and Dr. David Simpson (Carlsberg Laboratory, Copenhagen) for the kind gift of barley mutants.

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  1. Jan T. Svensson

    Present address: Department of Plant Biology and Biotechnology, VKR Center of Excellence Pro-Active Plants, University of Copenhagen, 1871, Frederiksberg C, Denmark

Authors and Affiliations

  1. CRA Genomic Research Centre, Via S. Protaso 302, 29017, Fiorenzuola d’Arda (PC), Italy

    Chiara Campoli, A. Michele Stanca, Luigi Cattivelli & Cristina Crosatti

  2. Laboratoire de Génétique et Biophysique des Plantes Département de Biologie, CEA, IBEB, SBVME, CNRS UMR Biologie Végétale et Microbiologie Environnemetales, Université Aix-Marseille II, 163, Avenue de Luminy, 13009, Marseille, France

    Stefano Caffarri

  3. Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

    Jan T. Svensson

  4. Dipartimento Scientifico e Tecnologico, Università di Verona, Strada Le Grazie 15, 37134, Verona, Italy

    Chiara Campoli & Roberto Bassi

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  1. Chiara Campoli
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Correspondence to Cristina Crosatti.

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Campoli, C., Caffarri, S., Svensson, J.T. et al. Parallel pigment and transcriptomic analysis of four barley Albina and Xantha mutants reveals the complex network of the chloroplast-dependent metabolism. Plant Mol Biol 71, 173–191 (2009). https://doi.org/10.1007/s11103-009-9516-8

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