Skip to main content

Advertisement

SpringerLink
Log in

Arabidopsis gun4 mutant have greater light energy transfer efficiency in photosystem II despite low chlorophyll content

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

Abstract

Arabidopsis gun4 mutant is defected in retrograde signaling and is characterized by reduced levels of chlorophyll. However, the impact of this mutation on plant photosynthetic performance remains unclear. We carried out a physiological characterization of gun4 in order to investigate the role of GUN4 for plant photosynthetic performance under light stress. The gun4 plants showed reduced minimal fluorescence in dark-adapted leaves and quantum yield of unregulated energy dissipation of photosystem II (PSII) under non-light-stress condition. The effective quantum yield of the PSII (ΦPSII) and photochemical quenching (qL) were higher in gun4 plants. Higher values of ΦPSII were also observed in gun4 under different light intensities. However, the rate of net carbon assimilation and stomatal conductance were lower in gun4. No differences were detected between the genotypes in the total absorption of 14CO2 as well as in the percentage of 14C flux to basic amino acids, sugars, starch, and cell wall. After light stress, the potential quantum yield of PSII decreased only in wild type and the non-photochemical quenching was higher in gun4. Taken together, the results suggest that gun4 transfers more efficiently the excess of light energy absorbed despite a reduction in chlorophyll and carotenoids content and has greater capacity to dissipate the excess of energy absorbed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ΦPSII :

Effective quantum yield of PSII

GUN:

Genome uncoupled

gun4 :

Genome uncoupled 4 mutant

LHCB:

Light harvesting chlorophyll binding proteins

LHC:

Light harvesting complex

LHCII:

Light harvesting complex of the complex II

Fm :

Maximal fluorescence in dark adapted leaves

Fo :

Minimal fluorescence in dark adapted leaves

MgChl:

Mg-chelatase enzyme

Mg-ProtoIX:

Mg-protoporphyrinIX

A :

Net photosynthetic rate

qN:

Non-photochemical quenching

ΦP :

Photochemical quantum yield of PSII

qL:

Photochemical quenching of lake model

PSII:

Photosystem II

Fv/Fm :

Potential quantum yield of PSII

ProtoIX:

ProtoporphyrinIX

ΦNO :

Quantum yield of non-regulated non-photochemical energy loss in PSII

g s :

Stomatal conductance

C i :

Substomatal CO2 concentration

E :

Transpiration

WT:

Wild type

References

  • Adhikari ND, Orler R, Chory J, Froehlich JE, Larkin RM (2009) Porphyrins promote the association of GENOMES UNCOUPLED 4 and Mg-chelatase subunit with chloroplast membranes. J Biolog Chem 284(37):24783–24796

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bilger W, Schreiber U (1986) Energy-dependent quenching of dark level chlorophyll fluorescence in intact leaves. Photosynth Res 10:303–308

    Article  CAS  PubMed  Google Scholar 

  • Bolhàr-Nordenkampf HR, Öquist GO (1993) Chlorophyll fluorescence as a tool in photosynthesis research. In: Hall DO, Scurlock JMO, Bolhàr-Nordenkampf HR, Leegood RC, Long SP (eds) Photosynthesis and production in a changing environment. Chapman & Hall, London, pp 193–205

    Google Scholar 

  • Brzezowski P, Schlicke H, Richter A, Dent RM, Niyogi KK, Grimm B (2014) The GUN4 protein plays a regulatory role in tetrapyrrole biosynthesis and chloroplast-tonucleus signalling in Chlamydomonas reinhardtii. Plant J. doi:10.1111/tpj.12560

    PubMed  Google Scholar 

  • Czarnecki O, Gläßer C, Chen JG, Mayer KFX, Grimm B (2012) Evidence for a contribution of ALA synthesis to plastid-to-nucleus signaling. Front Plant Sci 3:1–19

    Article  Google Scholar 

  • DaMatta FM, Cunha RL, Antunes WC, Martins SCV, Araujo WL, Fernie AR, Moraes GABK (2008) In field-grown coffee trees source–sink manipulation alters photosynthetic rates, independently of carbon metabolism, via alterations in stomatal function. New Phytol 178:348–357

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ortuño MF, Ribas-Carbo M, Diaz-Espejo A, Flórez-Sarasa ID, Medrano H (2007) Mesophyll conductance to CO2 in Arabidopsis thaliana. New Phytol 175:501–511

    Article  CAS  PubMed  Google Scholar 

  • Formighieri C, Ceol M, Bonente G, Rochaix JD, Bassi R (2012) Retrograde signaling and photoprotection in a gun4 mutant of Chlamydomonas reinhardtii. Mol Plant 5(6):1242–1262

    Article  CAS  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Hansson A, Jensen PE (2009) Chlorophyll limitation in plants remodels and balances the photosynthetic apparatus by changing the accumulation of photosystems I and II through two different approaches. Physiol Plant 135:214–228

    Article  CAS  PubMed  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu Z, Xu F, Guan L, Qian P, Liu Y, Zhang H, Huang Y, Hou S (2014) The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. J Exp Bot 65(4):1111–1123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115

    Article  CAS  PubMed  Google Scholar 

  • Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25(4):185–192

    Article  CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PSII quantum yield calculated from simple fluorescence parameters measured by PAM fluorometry and saturation pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Koussevitzky S, Nott TC, Mockler FH, Sachetto-Martins G, Surpin MJ, Chory J (2007) Multiple signals from damaged chloroplasts converge on a common pathway to regulate nuclear gene expression. Science 316:715–719

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Larkin RM, Ruckle ME (2008) Integration of light and plastid signals. Curr Opin Plant Biol 11:1–7

    Article  Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Wakao S, Fisher BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzimol 148:350–382

    Article  CAS  Google Scholar 

  • Masuda T, Fujita Y (2008) Regulation and evolution of chlorophyll metabolism. Photochem Photobiol Sci 7:1131–1149

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Mochizuki N, Brusslan JÁ, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelataseH subunit in plastid-nucleus signal transduction. Proc Natl Acad Sci USA 98:2053–2058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci USA 105:15184–15189

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 105:15178–15183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signalling. Annu Rev Plant Biol 57:739–759

    Article  CAS  PubMed  Google Scholar 

  • Obayashi T, Kinoshita K (2009) Rank of correlation coefficient as a comparable measure for biological significance of gene coexpression. DNA Res 16(2009):249–260

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res 37:D987–D991

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Obayashi T, Nishida K, Kasahara K, Kinoshita K (2011) ATTED-II updates: condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol 52:213–219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peter E, Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2(6):1198–1210

    Article  CAS  PubMed  Google Scholar 

  • Pfannschmidt T (2010) Plastidial retrograde signalling––a true ‘‘plastid factor’’ or just metabolite signatures? Trends Plant Sci 15:427–435

    Article  CAS  PubMed  Google Scholar 

  • Sobotka R, Dühring U, Komenda J, Peter E, Gardian Z, Tichy M, Grimm B, Wilde A (2008) Assembly of photosynthetic complexesprotein for chlorophyll metabolism and importance of the cyanobacterial Gun4. J Biol Chem 283:25794–25802

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Susek RE, Chory J (1992) A tale of two genomes: role of a chloroplast signal in coordinating nuclear and plastid genome expression. Aust J Plant Physiol 19:387–399

    Article  CAS  Google Scholar 

  • Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  CAS  PubMed  Google Scholar 

  • Teramoto H, Ono T, Minagawa J (2001) Identification of Lhcb gene family encoding the light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. Plant Cell Physiol 42:849–856

    Article  CAS  PubMed  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56(411):435–447

    Article  CAS  PubMed  Google Scholar 

  • Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571:119–123

    Article  CAS  PubMed  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV et al (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8):e718

    Article  PubMed Central  PubMed  Google Scholar 

  • Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28

    Article  CAS  PubMed  Google Scholar 

  • Zhang DP (2007) Signaling to the nucleus with a loaded GUN. Science 316:700–701

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Sawicki A, Willows RD, Luo M (2012) C-terminal residues of Oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis. FEBS Lett 586:205–210

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the CNPq (National Council for Technological and Scientific Development, Brazil) and FAPEMIG (Foundation for Research Assistance of the Minas Gerais State, Brazil). Scholarships granted by CNPq, CAPES and FAPEMIG are gratefully acknowledged. DMD was recipient of a scholarship from CAPES.

Author information

Authors and Affiliations

  1. Departamento de Biologia Vegetal, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Viçosa, Viçosa, MG, Brazil

    Danilo de Menezes Daloso, Werner Camargos Antunes, Téssio A. Santana, Daniela Pereira Pinheiro, Rogério Ferreira Ribas & Marcelo Ehlers Loureiro

  2. Departamento de Biologia, Universidade Estadual de Maringá, Maringá, Brazil

    Werner Camargos Antunes

  3. Centro de Ciências Agrárias, Ambientais e Biológicas, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, BA, Brazil

    Rogério Ferreira Ribas

  4. Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Gilberto Sachetto-Martins

Authors
  1. Danilo de Menezes Daloso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Werner Camargos Antunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Téssio A. Santana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniela Pereira Pinheiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rogério Ferreira Ribas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gilberto Sachetto-Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo Ehlers Loureiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo Ehlers Loureiro.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 281 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Daloso, D.M., Antunes, W.C., Santana, T.A. et al. Arabidopsis gun4 mutant have greater light energy transfer efficiency in photosystem II despite low chlorophyll content. Theor. Exp. Plant Physiol. 26, 177–187 (2014). https://doi.org/10.1007/s40626-014-0025-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-014-0025-z

Keywords

Search

Navigation