Periodic Reporting for period 4 - StressNetAdapt (Understanding evolutionary abiotic stress-network plasticity as foundation for new biotechnological strategies)
Période du rapport: 2020-02-01 au 2021-08-31
Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance:
A key achievement was the carefully controlled phenotypic comparison of three different brassicaceae species: Arabidopsis thaliana (Ath), Arabidopsis lyrata (Aly), and Eutrema salsugineum (Esa). We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations, and signaling network rewiring. In contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, abscisic acid signaling transcripts, and late growth responses. The stress sensitive Ath responds later than Aly and earlier than Esa, however its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath. Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance. (Marin et al., New Phytologist, 2019).
A key achievement was the carefully controlled phenotypic comparison of three different brassicaceae species: Arabidopsis thaliana (Ath), Arabidopsis lyrata (Aly), and Eutrema salsugineum (Esa). We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations, and signaling network rewiring. In contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, abscisic acid signaling transcripts, and late growth responses. The stress sensitive Ath responds later than Aly and earlier than Esa, however its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath. Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance. (Marin et al., New Phytologist, 2019).
To understand the underlying molecular differences in the gene regulatory network, we characterized the drought-induced Gene Regulatory Network (DGRN) that underlie differential drought response in the three species using a yeast-1-hybrid (Y1H) approach. We identified orthologs that showed divergent expression pattern under drought conditions using the transcriptome of the previous study. Ultimately, we cloned 141 promoters that include a set of 30 complete sets of orthologues, which we screened against a complete Ath transcription factor collection, yielding a regulatory network map consisting of 997 total and 543 distinct interactions that include 135 fully conserved interactions among the species. At the same time, 405 distinct interactions were only identified in a single or two of the three species indicating that these were modulated by the underlying evolutionary processes and are promising candidates for novel drought tolerance genes.
A further major achievement was the generation of a high-quality experimental map of the phytohormone signaling interactome network, in which the phytohormone abscisic acid plays a central role. Using our high-quality interactome mapping pipeline, we generated experimentally a systems-level map of the Arabidopsis phytohormone signaling-network consisting of more than 2,000 binary protein-protein interactions. In the highly interconnected network, pathway communities and hundreds of novel pathway contact points can be identified that represent potential points of crosstalk. Functional validation of candidates in seven hormone pathways demonstrate novel functions for 74% of tested proteins in 84% of candidate interactions, and indicate that a large majority of signaling proteins function pleiotropically in multiple pathways. Moreover, we identify several hundred largely small-molecule-dependent interactions of hormone receptors, especially for ABA receptors and their PP2C co-receptor. Comparison with previous reports suggests that non-canonical and non-transcription mediated receptor signaling is more common than currently appreciated. (Altmann et al., Extensive signal integration by the phytohormone protein network, Nature, 2020.)
Exploitation and dissemination of the results
Major publications:
Altmann M et al, Nature. 2020
Garcia VJ et al, Plant Cell 2020
Wierbowski SD et al, PNAS 2020
Marin-De La Rosa NA et al, New Phytol 2019
Garcia-Molina A,J Exp Bot. 2017
conferences and seminar series, e.g.:
Cold Spring Harbor Laboratory Meeting (CSHL): Network Biology, March 2019 & 2020
EMBO Workshop: International plant systems biology, April 2021
Conference in Roscoff/France: Systems Biology of Plants, August 2018
Forschungszentrum Jülich: HPPS Seminar, May 2018
Helmholtz Munich: Town Hall meeting, Institutes Seminars etc.
television report and interview
A further major achievement was the generation of a high-quality experimental map of the phytohormone signaling interactome network, in which the phytohormone abscisic acid plays a central role. Using our high-quality interactome mapping pipeline, we generated experimentally a systems-level map of the Arabidopsis phytohormone signaling-network consisting of more than 2,000 binary protein-protein interactions. In the highly interconnected network, pathway communities and hundreds of novel pathway contact points can be identified that represent potential points of crosstalk. Functional validation of candidates in seven hormone pathways demonstrate novel functions for 74% of tested proteins in 84% of candidate interactions, and indicate that a large majority of signaling proteins function pleiotropically in multiple pathways. Moreover, we identify several hundred largely small-molecule-dependent interactions of hormone receptors, especially for ABA receptors and their PP2C co-receptor. Comparison with previous reports suggests that non-canonical and non-transcription mediated receptor signaling is more common than currently appreciated. (Altmann et al., Extensive signal integration by the phytohormone protein network, Nature, 2020.)
Exploitation and dissemination of the results
Major publications:
Altmann M et al, Nature. 2020
Garcia VJ et al, Plant Cell 2020
Wierbowski SD et al, PNAS 2020
Marin-De La Rosa NA et al, New Phytol 2019
Garcia-Molina A,J Exp Bot. 2017
conferences and seminar series, e.g.:
Cold Spring Harbor Laboratory Meeting (CSHL): Network Biology, March 2019 & 2020
EMBO Workshop: International plant systems biology, April 2021
Conference in Roscoff/France: Systems Biology of Plants, August 2018
Forschungszentrum Jülich: HPPS Seminar, May 2018
Helmholtz Munich: Town Hall meeting, Institutes Seminars etc.
television report and interview
Droughts cause severe crop losses worldwide and climate change is projected to increase their prevalence in the future. Similar to the situation for many crops, the reference plant Arabidopsis thaliana (Ath) is considered drought-sensitive, whereas, as we demonstrate, its close relatives Arabidopsis lyrata (Aly) and Eutrema salsugineum (Esa) are drought-resistant. To understand the molecular basis for this plasticity we conducted a deep phenotypic, biochemical and transcriptomic comparison using developmentally matched plants. We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations and signaling network rewiring. By contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, ABA signaling transcripts and late growth responses. The stress-sensitive Ath responds later than Aly and earlier than Esa, although its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath. Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance.
This was an unexpected and in fact surprising finding. While these generally divergent drought response strategies are well known, it was surprising to see them implemented in such close relatives. This finding reemphasizes the enormous evolutionary plasticity of this trait.
Our findings published in 2020 (Nature) about extensive signal integration by the phytohormone protein network revealed, that a large majority of proteins mediates signaling by multiple hormones. That, the definition of a pathway may need to be completely revised and instead a network centric delocalized model of cellular information processing needs to be developed. This finding was neither planned nor anticipated and holds a great potential for further biotechnological developments including drought stress tolerance crop plants.
This was an unexpected and in fact surprising finding. While these generally divergent drought response strategies are well known, it was surprising to see them implemented in such close relatives. This finding reemphasizes the enormous evolutionary plasticity of this trait.
Our findings published in 2020 (Nature) about extensive signal integration by the phytohormone protein network revealed, that a large majority of proteins mediates signaling by multiple hormones. That, the definition of a pathway may need to be completely revised and instead a network centric delocalized model of cellular information processing needs to be developed. This finding was neither planned nor anticipated and holds a great potential for further biotechnological developments including drought stress tolerance crop plants.