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Klaus Apel
 &emdash;  Retired Faculty

Klaus Apel
Graduate Fields: Plant Biology


  • Blocking the Q -binding site of photosystem II by tenuazonic acid, a non-host-specific toxin of Alternaria alternata, activates singlet oxygen-mediated and EXECUTER-dependent signalling in Arabidopsis 2015

    Chen, S., Kim, C., Lee, J.M., Lee, H.A., Fei, Z., Wang, L., and Apel, K.
    Plant Cell Environ
  • Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity 2013

    Kim, C. and Apel, K.
    Photosynthesis Research 116,  455-464
    Full text...
  • O-1(2)-Mediated and EXECUTER-Dependent Retrograde Plastid-to-Nucleus Signaling in Norflurazon-Treated Seedlings of Arabidopsis thaliana 2013

    Kim, C.H. and Apel, K.
    Molecular Plant 6,  1580-1591
    Full text...
  • The SCO2 protein disulphide isomerase is required for thylakoid biogenesis and interacts with LHCB1 chlorophyll a/b binding proteins which affects chlorophyll biosynthesis in Arabidopsis seedlings 2012

    Tanz, S.K., Kilian, J., Johnsson, C., Apel, K., Small, I., Harter, K., Wanke, D., Pogson, B., and Albrecht, V.
    Plant J. 69,  743-75
    Full text...
  • The chloroplast division mutant caa33 of Arabidopsis thaliana reveals the crucial impact of chloroplast homeostasis on stress acclimation and retrograde plastid-to-nucleus signaling 2012

    Simkova, K., Kim, C., Gacek, K., Baruah, A., Laloi, C. and Apel, K.
    Plant J. 69,  701-712
    Full text...
  • Arabidopsis light-dependent protochlorophyllide oxidoreductase A (PORA) is essential for normal plant growth and development 2012

    Paddock, T., Lima, D., Mason, M.E., Apel, K. and Armstrong, G.A.
    Plant Mol. Biol. 78,  447-460
    Full text...
  • Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway 2012

    Kim, C., Meskauskiene, R., Zhang, S., Lee, K.P., Lakshmanan Ashok, M., Blajecka, K., Herrfurth, C., Feussner, I., and Apel, K.
    Plant Cell 24,  3026-3039
    Full text...
  • Arabidopsis light-dependent NADPH: protochlorophyllide oxidoreductase A (PORA) is essential for normal plant growth and development: an addendum 2012

    Kim, C. and Apel, K.
    Plant Mol. Biol. 80,  237-24
    Full text...
  • FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway 2012

    Kauss, D., Bischof, S., Steiner, S., Apel, K. and Meskauskiene, R.
    FEBS Lett. 586,  211-216
    Full text...
  • ‘happy on norflurazon’ (hon) mutations implicate perturbance of plastid homeostasis with activating stress acclimatization and changing nuclear gene expression in norflurazon-treated seedlings 2011

    Saini, G., Meskauskiene, R., Pijacka, W., Roszak, P., Sjogren, L.L.E., Clarke, A.K., Straus , M. and Apel, K.
    Plant J. 65,  690-702
    Full text...
  • Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development 2009

    Baruah, A., Simkova, K., Apel, K. and Laloi, C.
    Plant Mol. Biol. 70,  547-563
    Full text...
  • Modulation of O-1(2)-mediated retrograde signaling by the PLEIOTROPIC RESPONSE LOCUS 1 (PRL1) protein, a central integrator of stress and energy signaling 2009

    Baruah, A., Simkova, K., Hincha, D.K., Apel, K. and Laloi, C.
    Plant J. 60,  22-32
    Full text...
  • Characterization of soldat8, a Suppressor of Singlet Oxygen-Induced Cell Death in Arabidopsis Seedlings 2009

    Coll, N.S., Danon, A., Meurer, J., Cho, W.K. and Apel, K.
    Plant Cell Physiol. 50,  707-718
    Full text...
  • O-1(2)-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid 2009

    Kim, C., Lee, K.P., Baruah, A., Nater, M., Gobel, C., Feussner, I., and Apel, K.
    P. Natl. Acad. Sci. USA 106,  9920-9924
    Full text...
  • A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses 1O(2)-induced cell death 2009

    Meskauskiene, R., Wursch, M., Laloi, C., Vidi, P.A., Coll, N.S., Kessler, F., Baruah, A., Kim, C. and Apel, K.
    Plant J. 60,  399-410
    Full text...
  • No single way to understand singlet oxygen signalling in plants 2008

    Kim, C., Meskauskiene, R., Apel, K., and Laloi, C.
    EMBO Rep. 9,  435-439
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  • Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana 2007

    Laloi, C, Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K.
    P. Natl. Acad. Sci. USA 104,  672-677
    Full text...
  • EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana 2007

    Lee, K.P., Kim, C., Landgraf, F., and Apel, K.
    P. Natl. Acad. Sci. USA 104,  10270-10275
    Full text...
  • A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana 2006

    Laloi, C., Przybyla, D., and Apel, K.
    J. Exp. Bot. 57,  1719-1724
    Full text...
  • Reactive oxygen signalling: the latest news 2004

    Laloi, C., Apel, K., and Danon, A.
    Curr. Opin. Plant Biol. 7,  323-328
    Full text...
  • The Genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana 2004

    Wagner, D., Przybyla, D., op den Camp, R., Kim, C., Landgraf, F., Lee, K.P., Wursch, M., Laloi, C., Nater, M., Hideg, E., and Apel, K.
    Science 306,  1183-1185
    Full text...
  • Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis 2003

    op den Camp, R.G., Przybyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Gobel, C., Fuessner, I., Nater, M., and Apel, K.
    Plant Cell 15,  2320-2332
    Full text...

Intern Projects

Identification of genes involved in stress signaling.

Our research is aimed at understanding how plants are able to respond to environmental stress conditions. In particular we are interested in responses of plants to stress conditions that impede photosynthesis such as drought, high light or high or low temperature. Under these conditions chloroplasts start to accumulate reactive oxygen species that may damage the cell but may also be  perceived as signals that activate the plants’ stress resistance. We have analyzed a signaling pathway that is activated in chloroplasts by one of the reactive oxygen species, singlet oxygen, and have identified constituents of this signaling pathway that will allow us to modulate the plant’s response to stress and enhance its stress resistance.



    • Technology Area: Flowering
    • Title: Combination of genes for the regulation of the induction of flowering in useful and ornamental plants
    • US Patent/Application(s): 11/200,465
    • Publication: Plant J 2000Plant J 19999

Research Overview

Professor Klaus Apel was a member of the faculty at BTI from 2008 – 2016. He has returned to the Swiss Federal Institute of Technology in Zurich, where he is a professor emeritus.

Learn more about his life and work in this profile of Klaus Apel.

How do plants respond to environmental stress?

Plants can endure extreme environmental stress (heat, drought, cold or intense light) through genetically controlled defenses, such as wilting, loss of leaves or stunted growth, but these very defenses can also reduce yields, among other effects. As a result, one effect of global warming could be reduced food production just when the world’s population is burgeoning. Understanding how plants sense and respond to stress at the genetic level is the ultimate objective of Klaus Apel’s laboratory at BTI. His findings could enable scientists to mitigate the negative results of stress, such as yield loss, or fine tune a plant’s ability to survive climate change.

It turns out that chloroplasts — the tiny organs that contain chlorophyll and carry out photosynthesis — play an important role in a plant’s ability to sense environmental stress. Conditions such as drought, heat, cold and intense light interfere with the normal photosynthetic process in the chloroplasts, which leads to over-production of sometimes toxic forms of oxygen, called reactive oxygen species (ROS). High levels of ROS were previously considered detrimental to the cell. However, recent work with an Arabidopsis thaliana mutant by Apel and his research group indicates that the release of one type of ROS, called singlet oxygen, in the chloroplast actually triggers a variety of positive stress adaptation responses in the plant. These responses include slowed plant growth, cell death, and the activation of a broad range of defense genes, which normally are turned on only in the presence of pathogens.

In further work, Apel’s group proved that certain genetic mutations in Arabidopsis eliminate the plant’s stress responses without interfering with the release of singlet oxygen. It appears these mutations prevent the plant from sensing the presence of singlet oxygen, which in turn prevents symptoms of stress. Apel’s group has identified these mutated genes, which is a first and crucial step toward understanding the genetic basis of the stress response in plants. The results of Apel’s work could lead to plants that cope better with the environmental stress of global warming. Ultimately, such a discovery could help increase food supplies or predict a plant’s susceptibility to environmental changes.

FLU: A negative regulator of chlorophyll biosynthesis

One of the first reactions of plants under stress is the enhanced production of chemically distinct reactive oxygen species (ROS). A major difficulty in elucidating the biological activity of ROS during stress stems from the fact that not only one but several chemically distinct ROS are generated simultaneously, thus making it very difficult to link a particular stress response to a specific ROS. This problem has been alleviated by using the conditional flu mutant of Arabidopsis that allows the production of only singlet oxygen within plastids in a non-invasive, controlled manner.

In the dark the flu mutant accumulates protochlorophyllide (Pchlide), a potent photosensitizer that upon illumination generates singlet oxygen. Several singlet oxygen-mediated stress responses have been distinguished during re-illumination of the flu mutant. Furthermore, inactivation of nuclear genes encoding the two closely related plastid proteins Executer1 and Executer2 has been shown to be sufficient to abrogate these stress responses despite the ongoing release of singlet oxygen. By varying the length of the dark period, one can adjust the level of the photosensitizer Pchlide and define conditions that minimize the cytotoxicity of singlet oxygen: either endorse acclimation in flu plants exposed to a very short dark period as one extreme, or promote a genetically controlled cell death response in plants shifted for a longer period in the dark as another extreme.

This activity of singlet oxygen assigns a new function to the chloroplast, namely that of a sensor of environmental changes that activates a broad range of stress responses known to be activated also by abiotic and biotic stressors. This work is aimed at dissecting the complexity of singlet oxygen signaling and understanding and eventually also modifying the genetic constraints that determine the adaptability of plants to environmental changes.