Systems biology of drought tolerance in Arabidopsis
With the rapidly growing world population and the increasing demand for food, the importance to stabilize plant yield even under adverse environmental conditions is evident.
One of the most destructive factors for worldwide agriculture is drought stress. As illustrated by the drought period of summer of 2015, drought stress in moderate climates does not often threaten the plants survival, but has a clear negative impact on plant growth. Even when the water availability is only slightly decreased, mechanisms are rapidly induced to repress plant growth (Claeys et al., 2014). Understanding this growth inhibition at molecular level forms a first major step towards future engineering of plants with reduced yield penalties under drought.
With this ultimate goal in mind, our group explores the mechanisms underlying leaf growth inhibition in Arabidopsis by exposing plants to in vitro medium supplemented with an osmotic compound, in order to mimic drought stress. Our past research enabled to uncover that:
- The response to stress occurs extremely rapidly (Skirycz et al., 2011a).
- This response is highly depending on the stress level (Skirycz et al., 2011b; Claeys et al., 2014),
- and on the developmental stage of the studied organ (Skirycz et al., 2010).
- The plant hormones ethylene and gibberellins are important in the young leaves of plants exposed to stress.
Specifically in these young, actively growing leaves, ethylene triggers a very fast response involving several ETHYLENE RESPONSE FACTORs (ERFs) and, a bit later, repression of the GA-pathway is causing inhibition of the growth machinery (Claeys et al., 2012). To explore the molecular connection between ethylene and GA, we opt for the routinely-used in vitro osmotic stress assays, as they offer multiple advantages to uncover such rapid responses. We identified ERF6 as a central regulator of leaf growth under stress and showed that ERF6 regulates the inactivation of the growth-stimulating GA-pathway but also induces multiple other transcription factors involved in stress response (Dubois et al., 2013). In total, we identified 20 transcription factors around ERF6, and observed that these transcription factors are regulating each other’s expression, thereby forming a dense and complex transcriptional network. It is now our aim to use mathematical modeling to unravel the dynamics of this network under stress and to link the status of the network to leaf growth (Lisa Van den Broeck). As a first piece of this puzzle, the regulatory relationship between two transcription factors of this network, ERF6 and ERF11, was recently characterized (Dubois et al., 2015). To extend the network even further, without a bias towards transcription factors, we are performing a large scale forwards genetics screen for new genes potentially involved in leaf growth regulation under stress (Ting Li).
Besides the in vitro work, we also aim to unravel the growth-regulatory pathways active under in soil mild drought stress. We use the Weighing, Imaging and Watering Machine (WIWAM) to establish an appropriate setup enabling the capture of early drought responses in actively growing Arabidopsis leaves, by tracking leaf growth over time and measuring expression changes with a high time-resolution. Growth and transcriptional responses to in soil drought are extremely complex, with the time of day as a crucial factor influencing the extent, the specificity and sometimes also the direction of the expression changes. While the response to in soil drought does not seem to involve the same molecular players as under in vitro stress, the general mechanisms, including ethylene- and gibberellin-mediated growth inhibition, are most likely conserved. We also make use of the genetic variation in Arabidopsis to identify new genes potentially involved in the response to mild drought by means of transcriptomic and genome-wide association studies (Clauw et al, 2015).
People involved: Nathalie Gonzalez (project leader), Pieter Clauw, Marieke Dubois, Lisa Van den Broeck and Li Ting
Dubois M, Van den Broeck L, Claeys H, Van Vlierberghe K, Matsui M, Inzé D. (2015) The ETHYLENE RESPONSE FACTORS ERF6 and ERF11 antagonistically regulate mannitol-induced growth inhibition in Arabidopsis. Plant Physiol. PMID: 25995327
Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, Storme V, Clement L, Gonzalez N, Inzé D. (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol. PMID: 25604532
Claeys H, Van Landeghem S, Dubois M, Maleux K, Inzé D. (2014) What Is Stress? Dose-Response Effects in Commonly Used in Vitro Stress Assays. Plant Physiol PMID: 24710067
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, Vanden Bossche R, De Milde L, Yoshizumi T, Matsui M, Inzé D.(2013) Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol. 162(1):319-32
Claeys H., Skirycz, A., Maleux, K., Inzé, D. (2012) DELLA Signaling Mediates Stress-Induced Cell Differentiation in Arabidopsis Leaves through Modulation of Anaphase-Promoting Complex/Cyclosome Activity. Plant Physiol. 159(2):739-47.
Skirycz, A., Vandenbroucke, K., Clauw, P., Maleux, K., De Meyer, B., Dhondt, S., Pucci, A., Gonzalez, N., Hoeberichts, F., Tognetti V.B., Galbiati, M., Tonelli, C., Van Breusegem, F., Vuylsteke, M., Inzé, D. (2011b) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotechnol. 29(3):212-4.
Skirycz, A., Claeys, H., De Bodt, S., Oikawa, A., Shinoda, S., Andriankaja, M., Eloy, N.B., Coppens, F., Yoo, S.D., Saito, K., Inzé, D. (2011a) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell. 23(5):1876-88.
Skirycz, A., Inzé, D. (2010) More from less: plant growth under limited water. Curr Opin Biotechnol. 21(2):197-203.
Skirycz, A., De Bodt, S., Obata, T., De Clercq, I., Claeys, H., De Rycke, R., Andriankaja, M., Van Aken, O., Van Breusegem, F., Fernie, A.R., Inzé, D. (2010) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiol. 152(1):226-44.