Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants

Marcus Jansen A , Frank Gilmer A , Bernhard Biskup A , Kerstin A. Nagel A , Uwe Rascher A , Andreas Fischbach A , Sabine Briem A , Georg Dreissen A , Susanne Tittmann A , Silvia Braun A , Iris De Jaeger B , Michael Metzlaff B , Ulrich Schurr A , Hanno Scharr A and Achim Walter A C
+ Author Affliations
- Author Affliations

A Institute of Chemistry and Dynamics of the Geosphere ICG-3 (Phytosphere), Forschungszentrum Jülich GmbH, 52425 Jülich, Germany.

B Bayer BioScience N.V., Technologiepark 38, 9052 Gent, Belgium.

C Corresponding author. Email: a.walter@fz-juelich.de

This paper originates from a presentation at the 1st International Plant Phenomics Symposium, Canberra, Australia, April 2009.

Functional Plant Biology 36(11) 902-914 https://doi.org/10.1071/FP09095
Submitted: 30 April 2009  Accepted: 3 August 2009   Published: 5 November 2009

Abstract

Stress caused by environmental factors evokes dynamic changes in plant phenotypes. In this study, we deciphered simultaneously the reaction of plant growth and chlorophyll fluorescence related parameters using a novel approach which combines existing imaging technologies (GROWSCREEN FLUORO). Three different abiotic stress situations were investigated demonstrating the benefit of this approach to distinguish between effects related to (1) growth, (2) chlorophyll-fluorescence, or (3) both of these aspects of the phenotype. In a drought stress experiment with more than 500 plants, poly(ADP-ribose) polymerase (PARP) deficient lines of Arabidopsis thaliana (L.) Heynh showed increased relative growth rates (RGR) compared with C24 wild-type plants. In chilling stress, growth of PARP and C24 lines decreased rapidly, followed by a decrease in Fv/Fm. Here, PARP-plants showed a more pronounced decrease of Fv/Fm than C24, which can be interpreted as a more efficient strategy for survival in mild chilling stress. Finally, the reaction of Nicotiana tabacum L. to altered spectral composition of the intercepted light was monitored as an example of a moderate stress situation that affects chlorophyll-fluorescence related, but not growth-related parameters. The examples investigated in this study show the capacity for improved plant phenotyping based on an automated and simultaneous evaluation of growth and photosynthesis at high throughput.

Additional keywords: chilling stress, drought, dynamic processes, image processing, Nicotiana tabacum, PARP, phenomics.


Acknowledgements

B. Biskup and S. Tittmann acknowledge support of their PhD theses by the Heinrich-Heine University of Düsseldorf, Germany. We are grateful to I.-L. Lai and R. Poiré for testing earlier versions of the setup in preliminary experiments and to B. Uhlig, M. Schmitz and B. Greve for assisting in plant cultivation. We thank K.H. Kjaer and S. Matsubara for constructive comments on earlier versions of this manuscript.


References


Adams WW, Demmig-Adams B, Verhoeven AS, Barker DH (1995) ‘Photoinhibition’ during winter stress – involvement of sustained xanthophyll cycle-dependent energy dissipation. Australian Journal of Plant Physiology 22, 261–276.
CrossRef | CAS | open url image1

Allen DJ, Nogues S, Baker NR (1998) Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis? Journal of Experimental Botany 49, 1775–1788.
CrossRef | CAS | open url image1

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
CrossRef | CAS | PubMed | open url image1

Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. Journal of Experimental Botany 55, 1607–1621.
CrossRef | CAS | PubMed | open url image1

Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiology 132, 485–493.
CrossRef | CAS | PubMed | open url image1

Berglund T (1994) Nicotinamide, a missing link in the early stress-response in eukaryotic cells – a hypothesis with special reference to oxidative stress in plants. FEBS Letters 351, 145–149.
CrossRef | CAS | PubMed | open url image1

Biskup B, Scharr H, Fischbach A, Wiese-Klinkenberg A, Schurr U, Walter A (2009) Diel growth cycle of isolated leaf discs analyzed with a novel, high-throughput three-dimensional imaging method is identical to that of intact leaves. Plant Physiology 149, 1452–1461.
CrossRef | CAS | PubMed | open url image1

Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
CrossRef | PubMed | open url image1

Butler WL (1978) Energy-distribution in photo-chemical apparatus of photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 29, 345–378.
CAS |
open url image1

Chaerle L, Van Der Straeten D (2001) Seeing is believing: imaging techniques to monitor plant health. Biochimica et Biophysica Acta 1519, 153–166.
CAS | PubMed |
open url image1

De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. The Plant Journal 41, 95–106.
CrossRef | CAS | PubMed | open url image1

Ehlert B, Hincha D (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4, 12.
CrossRef | PubMed | open url image1

Fiscus EL, Booker FL (1995) Is increased UV-B a threat to crop photosynthesis and productivity? Photosynthesis Research 43, 81–92.
CrossRef | CAS | open url image1

Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
CAS |
open url image1

Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences of the United States of America 97, 11098–11101.
CrossRef | CAS | PubMed | open url image1

Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M , et al . (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist 169, 623–635.
CrossRef | PubMed | open url image1

Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: ‘PAR-laying’ NAD(+) into a nuclear signal. Genes & Development 19, 1951–1967.
CrossRef | CAS | PubMed | open url image1

Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends in Plant Science 6, 262–267.
CrossRef | CAS | PubMed | open url image1

Leister D, Varotto C, Pesaresi P, Niwergall A, Salamini F (1999) Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiology and Biochemistry 37, 671–678.
CrossRef | CAS | open url image1

Lepiniec L, Babiychuk E, Kushnir S, Vanmontagu M, Inze D (1995) Characterization of an Arabidopsis thaliana cDNA homolog to animal poly(ADP-Ribose) polymerase. FEBS Letters 364, 103–108.
CrossRef | CAS | PubMed | open url image1

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
CrossRef | CAS | PubMed | open url image1

Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15–19.
CrossRef | CAS | PubMed | open url image1

Montes JM, Melchinger AE, Reif JC (2007) Novel throughput phenotyping platforms in plant genetic studies. Trends in Plant Science 12, 433–436.
CrossRef | CAS | PubMed | open url image1

Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
CAS | CrossRef | PubMed |
open url image1

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
CrossRef | CAS | PubMed | open url image1

Öquist G, Huner NP (2003) Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology 54, 329–355.
CrossRef | PubMed | open url image1

Osmond CB, Daley PF, Badger MR, Lüttge U (1998) Chlorophyll fluorescence quenching during photosynthetic induction in leaves of Abutilon striatum Dicks. infected with Abutilon mosaic virus, observed with a field-portable imaging system. Botanica Acta 111, 390–397.
CAS |
open url image1

Pearce RS (1999) Molecular analysis of acclimation to cold. Plant Growth Regulation 29, 47–76.
CrossRef | CAS | open url image1

Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment 32, 237–249.
CrossRef | CAS | PubMed | open url image1

Rongvaux A, Andris F, Van Gool F, Leo O (2003) Reconstructing eukaryotic NAD metabolism. BioEssays 25, 683–690.
CrossRef | CAS | PubMed | open url image1

Rozema J, van de Staaij J, Björn LO, Caldwell M (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology & Evolution 12, 22–28.
CrossRef | open url image1

Satoh MS, Poirier GG, Lindahl T (1994) Dual function for poly(ADP-Ribose) synthesis in response to DNA strand breakage. Biochemistry 33, 7099–7106.
CrossRef | CAS | PubMed | open url image1

Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 279–309. (Springer-Verlag: Dordrecht, The Netherlands)

Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nature Reviews. Molecular Cell Biology 7, 517–528.
CrossRef | CAS | PubMed | open url image1

Schurr U, Walter A, Rascher U (2006) Functional dynamics of plant growth and photosynthesis–from steady-state to dynamics – from homogeneity to heterogeneity. Plant, Cell & Environment 29, 340–352.
CrossRef | CAS | PubMed | open url image1

Scovassi AI, Izzo R, Franchi E, Bertazzoni U (1986) Structural analysis of poly(ADP-ribose) polymerase in higher and lower eukaryotes. European Journal of Biochemistry 159, 77–84.
CrossRef | CAS | PubMed | open url image1

Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296–302.
CrossRef | CAS | PubMed | open url image1

Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5, 537–542.
CrossRef | CAS | PubMed | open url image1

Tsormpatsidis E, Henbest RGC, Davis FJ, Battey NH, Hadley P, Wagstaffe A (2008) UV irradiance as a major influence on growth, development and secondary products of commercial importance in Lollo Rosso lettuce ‘revolution’ grown under polyethylene films. Environmental and Experimental Botany 63, 232–239.
CrossRef | CAS | open url image1

Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proceedings of the National Academy of Sciences of the United States of America 104, 15150–15155.
CrossRef | CAS | PubMed | open url image1

Walter A, Rascher U, Osmond B (2004) Transitions in photosynthetic parameters of midvein and interveinal regions of leaves and their importance during leaf growth and development. Plant Biology 6, 184–191.
CrossRef | CAS | PubMed | open url image1

Walter A, Scharr H, Gilmer F, Zierer R, Nagel KA , et al . (2007) Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species. New Phytologist 174, 447–455.
CrossRef | PubMed | open url image1

Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 60, 279–304.
CrossRef | CAS | PubMed | open url image1

Walters RG, Shephard F, Rogers JJM, Rolfe SA, Horton P (2003) Identification of mutants of Arabidopsis defective in acclimation of photosynthesis to the light environment. Plant Physiology 131, 472–481.
CrossRef | CAS | PubMed | open url image1

Woo N, Badger M, Pogson B (2008) A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Methods 4, 27.
CrossRef | PubMed | open url image1

Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. The Plant Cell 14, S165–S183.
CAS | CrossRef | PubMed |
open url image1

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
CrossRef | CAS | PubMed | open url image1








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