GRK 1525:  The Dynamic Response of Plants to a Changing Environment

• Subject Area: Plant Sciences
• Term: from 2009 to 2018
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 65369579

• Final Report Year: 2019

Final Report Abstract

Plants are sessile organisms and hence, in contrast to, e.g., animals cannot evade shorter or permanent episodes of stress by flight. In contrast, plants must mount a rapid and effective response to temporarily adapt to stress, be it abiotic, such as drought, heat, or excess light, or biotic, such as pathogen attack, to survive the stressful situation. This short-term acclimation enables survival and hence the basis for reproductive success. Reproductive success, in turn, is a strict prerequisite to adaptation to longer-term environmental stress, such as altered growth temperatures and precipitation patters due to, e.g., climate change. Long-term adaptation occurs at the level of the genome under the mechanisms of evolution by natural selection. In its first funding phase, IRTG 1525 "The dynamic response of plants to a changing environment" concentrated on rapid cellular and developmental acclimation responses to environmental stress, such as high light and suboptimal growth temperatures, with a strong focus on abiotic stress factors. Major findings included a molecular understanding of the mechanisms underpinning the dissipation of excess light energy through the activation of non-photochemical quenching by the PsbS protein, posttranslational regulation of the plant stem cell niche by protein phosphorylation, or the control of response to the environment by the circadian clock. In transition to the second funding cycle, the IRTG also considered biotic stressors, such as pathogen attack and it included adaptation to altered environments by genome evolution. Major findings included a new understanding of how plants communicate the attack by bacteria from infected to non-infected leaves and thereby induce immunity in the non-infected leaves. Computational simulations of metabolic evolution provided exciting and novel insights into the mechanisms underpinning the evolution of C4 photosynthesis via C3-C4 intermediate stages. The IRTG provided large scale datasets, such as comprehensive transcriptomic atlases and genome sequences that are of significant interest to the broader scientific community. The scientific program of the IRTG was enabled by interdisciplinary research at the interface between experimental plant science and computational biology. This provided a rich training environment for IRTG’s graduate and postdoctoral researchers, preparing them for a multitude of career opportunities in life science research. The IRTG implemented novel forms of graduate training at HHU, such as a Fast Track PhD program that is open to excellent students holding a BSc degree. With a strong emphasis on training in quantitative biology, statistics, and computational biology the IRTG prepared its graduates for careers in datadriven and large-scale biology. All graduate students stayed for a minimum of six months in the laboratories of partnering groups at Michigan State University, under the guidance of local faculty mentors. These interactions led to a significant number of joint publications and enriched the training experience of the participating students with an international perspective.

Publications

• (2009) A signalling module controlling the stem cell niche in Arabidopsis root meristems. Current Biology 19, 909-914
  Stahl Y, Wink R, Ingram G, Simon R
  (See online at https://doi.org/10.1016/j.cub.2009.03.060)
• (2011) An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiology 155 (1): 142-156
  Bräutigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, Weber KL, Carr KM, Gowik U, Maß J, Lercher MJ, Westhoff P, Hibberd JM, Weber AP
  (See online at https://doi.org/10.1104/pp.110.159442)
• (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23: 1-13
  Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber APM
  (See online at https://doi.org/10.1105/tpc.111.090324)
• (2012) Aberrant temporal growth pattern and morphology of root and shoot caused by a defective circadian clock in Arabidopsis thaliana. Plant Journal 72 (1): 154-61
  Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A
  (See online at https://doi.org/10.1111/j.1365-313x.2012.05073.x)
• (2012) Agrobacteriummediated Arabidopsis thaliana transformation: An overview of T-DNA binary vectors, floral dip and screening for homozygous lines. Endocytobiosis Cell Res 22: 19-28
  Bernhardt K, Vigelius SK, Wiese J, Linka N, Weber APM
  
• (2012) Cutoffs and k-mers: implications from a transcriptome study in allopolyploid plants. BMC Genomics 13: 92
  Gruenheit N, Deusch O, Esser C, Becker M, Voelckel C, Lockhart P
  (See online at https://doi.org/10.1186/1471-2164-13-92)
• (2012) Diel growth rhythms in plants - Circadian control and environmental response
  Ruts, Tom
  
• (2012) Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response? J Exp Botany 63 (9): 3339 – 51
  Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A
  (See online at https://doi.org/10.1093/jxb/err334)
• (2012) Microtubule-dependent membrane dynamics in Ustilago maydis: Trafficking and function of Rab5a-positive endosomes. Commun Integr Biol 5: 485-90
  Göhre V, Vollmeister E, Bölker M, Feldbrügge M
  (See online at https://doi.org/10.4161/cib.21219)
• (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. MPMI 25: 1083-92
  Göhre V, Jones AME, Sklenář J, Robatzek S, Weber APM
  (See online at https://doi.org/10.1094/mpmi-11-11-0301)
• (2012) Natural genetic variation in the expression regulation of the chloroplast antioxidant system among Arabidopsis thaliana accessions. Physiol Plant 146: 53-70
  Juszczak I, Rudnik R, Pietzeniuk B, Baier M
  (See online at https://doi.org/10.1111/j.1399-3054.2012.01602.x)
• (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24: 5123-41
  Návarová H, Bernsdorff F, Döring A-C, Zeier J
  (See online at https://doi.org/10.1105/tpc.112.103564)
• (2012) The leaf reticulate mutant dov1 is impaired in the first step of purine metabolism. Mol Plant 5: 1227-1241
  Rosar C, Kanonenberg K, Nanda AM, Mielewczik M, Bräutigam A, Novák O, Strnad M, Walter A, Weber APM
  (See online at https://doi.org/10.1093/mp/sss045)
• (2012) The strength of the miR398-Csd2-CCS1 regulon is subject to natural variation in Arabidopsis thaliana. FEBS Lett. 586(19):3385-90
  Juszczak I, Baier M
  (See online at https://doi.org/10.1016/j.febslet.2012.07.049)
• (2012) Transport proteins regulate the flux of metabolites and cofactors across the membrane of plant peroxisomes. Frontiers in Plant Sci 3:3 eCollection 2012
  Linka N, Esser C
  (See online at https://doi.org/10.3389/fpls.2012.00003)
• (2013) An engineered plant peroxisome and its application in biotechnology. Plant Sci 210:232- 40
  Kessel-Vigelius SK, Wiese J, Schroers MG, Wrobel TJ, Hahn F, Linka N
  (See online at https://doi.org/10.1016/j.plantsci.2013.06.005)
• (2013) C4 photosynthesis: from evolutionary analyses to strategies for synthetic reconstruction of the trait. Curr Opin Plant Biol 16 (3): 315-21
  Denton AK, Simon R, Weber APM
  (See online at https://doi.org/10.1016/j.pbi.2013.02.013)
• (2013) Co-expression analysis as tool for the discovery of transport proteins in photorespiration. Plant Biol 15 (4): 686-93
  Bordych C, Eisenhut M, Pick TR, Külahoglu C, Weber APM
  (See online at https://doi.org/10.1111/plb.12027)
• (2013) Evolution of C4 Phosphoenolpyruvate Carboxylase - enhanced feedback inhibitor tolerance is determined by a single residue. Mol Plant 6 (6):1996 -9
  Paulus JK, Niehus C, Groth G
  (See online at https://doi.org/10.1093/mp/sst078)
• (2013) Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution. Nature Commun 4:1518
  Paulus JK, Schlieper D, Groth G
  (See online at https://doi.org/10.1038/ncomms2504)
• (2013) Kristallisation und vergleichende Strukturuntersuchung der Phosphoenolpyruvat Carboxylase aus der C3 Pflanze Flaveria pringlei und der C4 Pflanze Flaveria trinervia
  Paulus, Judith Katharina
  
• (2013) Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes. Current Biology 23 (5): 362- 71
  Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S, Gustavo Pinto K, Kirschner GK, Schmid JB, Wink RH, Hülsewede A, Felekyan S, Seidel CAM, Simon R
  (See online at https://doi.org/10.1016/j.cub.2013.01.045)
• (2013) On the function of peptide signaling pathways in the root meristem of Arabidopsis thaliana
  Wink, René Hendrik
  
• (2013) Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell 153, 1579-1588
  Heckmann D, Schulze S, Denton A, Gowick U, Westhoff P, Weber APM, Lercher M
  (See online at https://doi.org/10.1016/j.cell.2013.04.058)
• (2013) Synchronous high-resolution phenotyping of leaf and root growth in Nicotiana tabacum over 24h periods with GROWMAP-plant. Plant Methods 9: 2
  Ruts T, Matsubara S, Walter A
  (See online at https://doi.org/10.1186/1746-4811-9-2)
• (2013) The genome of Tarenaya hassleriana provides insights into reproductive trait and genome evolution of crucifers. Plant Cell (8): 2813-30
  Cheng S, van den Bergh E, Zeng P, Zhong X, Xu J, Liu X, Hofberger J, de Bruijn S, Bhide AS, Külahoglu C, Bian C, Chen J, Fan G, Kaufmann K, Hall JC, Becker A, Bräutigam A, Weber APM, Shi C, Zheng Z, Li W, Lv M, Wang J, Zou H, Quan Z, Hibberd JM, Zhang G, Zhu XG, Xu X, Schranz E
  (See online at https://doi.org/10.1105/tpc.113.113480)
• (2013) Toward intracellular membrane Transport- Characterization of the Mitochondrial Carrier Family in Plants
  Keßel-Vigelius, Sarah Katharina
  
• (2014) Azolla domestication towards a biobased economy? Transcriptome database and methods for dissemination, cross fertilization, and storage of Azolla fllliculoides. New Phytol 202(3): 1069-1082
  Brouwer P, Bräutigam A, Külahoglu C, Tazelaar A, Kurz S, Nierop K, van der Werf A, Weber APM, Schluepmann H
  (See online at https://doi.org/10.1111/nph.12708)
• (2014) Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C3 and C4 plant species. Plant Cell, 26(8):3243-60
  Külahoglu C, Denton AK, Sommer M, Maß J, Schliesky S, Wrobel TJ, Berckmans B, Gongora-Castillo E, Buell CR, Simon R, De Veylder L, Bräutigam A, Weber APM
  (See online at https://doi.org/10.1105/tpc.114.123752)
• (2014) Direct and selective small-molecule inhibition of photosynthetic PEP carboxylase: New approach to combat C4 weeds in arable crops. FEBS Lett. 5;588(12):2101-6
  Paulus JK, Förster K, Groth G
  (See online at https://doi.org/10.1016/j.febslet.2014.04.043)
• (2014) In planta inactivation of the C4 phosphoenolpyruvate carboxylase (PEPC) gene of Flaveria bidentis and evolutionary analyses of the PEPC protein kinase (PPCK) gene family of Flaveria
  Aldous, Sophia Hilary
  
• (2014) Mathematical modelling of metabolism applied to the evolution of photosynthesis
  Heckmann, David
  
• (2014) Propionate metabolism in yeast and plants
  Wiese, Jan
  
• (2014) Quantitative transcriptome analysis using RNA- seq. Methods Mol Biol. 1158:71-91
  Külahoglu C and Bräutigam A
  (See online at https://doi.org/10.1007/978-1-4939-0700-7_5)
• (2014) Resolving the activation site of positive regulators in plant phosphoenolpyruvate carboxylase, Mol Plant 7(2):437 – 40
  Schlieper D, Foerster K, Paulus JK, Groth G
  (See online at https://doi.org/10.1093/mp/sst130)
• (2014) The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife 3:e02478
  Mallmann J, Heckmann D, Bräutigam A, Lercher MJ, Weber APM, Westhoff P, Gowik U
  (See online at https://doi.org/10.7554/elife.02478)
• (2014) Towards an integrative model of C4 photosynthetic subtypes – insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. J Exp Bot 65(13):3579-93
  Bräutigam A, Schliesky S, Külahoglu C, Osborne C, Weber APM
  (See online at https://doi.org/10.1093/jxb/eru100)
• (2014): Evolution of the phosphoenolpyruvate carboxylase protein kinase family in C3 and C4 Flaveria species. Plant Physiol 165(3):1076-1091
  Aldous SA, Weise SE, Sharkey TD, Waldera-Lupa DM, Stühler K, Malmann J, Groth G, Gowik U, Westhoff P, Arsova B
  (See online at https://doi.org/10.1104/pp.114.240283)
• (2015) "Chitinases are essential for cell separation in Ustilago maydis". Eukaryotic Cell 14(9):846-57
  Langner T, Öztürk M, Hartmann S, Cord-Landwehr S, Moerschbacher B, Walton JD, Göhre V
  (See online at https://doi.org/10.1128/ec.00022-15)
• (2015) Asymmetric cell divisions constructing Arabidopsis stem cell niches: the emerging role of protein phosphatases. Plant Biol (Stuttg). Sep;17(5):935- 45
  Boyer F, Simon R
  (See online at https://doi.org/10.1111/plb.12352)
• (2015) Charakterisierung der chitinolytischen Maschinerie aus Ustilago maydis
  Langner, Thorsten
  
• (2015) Establishment of C4 Photosynthesis in Ontogeny and Evolution
  Denton, Alisandra Kaye
  
• (2015) Mathematical modelling of WOX5-and CLE40- mediated columella stem cell homeostasis in Arabidopsis. J Exp Bot. Aug;66(17):5375-84
  Richards S, Wink RH, Simon R
  (See online at https://doi.org/10.1093/jxb/erv257)
• (2015) Modelling metabolic evolution on phenotypic fitness landscapes: a case study on C4 photosynthesis. Biochem Soc Trans. Dec;43(6):1172-6
  Heckmann D
  (See online at https://doi.org/10.1042/bst20150148)
• (2015) On the role of amino acids in plant disease resistance: Interplay between pipecolic acid and salicylic acid in plant systemic acquired resistance
  Bernsdorff, Friederike Elisabeth Maria
  
• (2015) Retained duplicate genes in green alga Chlamydomonas reinhardtii tend to be stress responsive and experience frequent response gains. BMC Genomics. 16:149
  Wu G, Hufnagel DE, Denton AK, Shiu SH
  (See online at https://doi.org/10.1186/s12864-015-1335-5)
• (2015) The role of the PsbS protein in the regulation of energy dissipation in vascular plants and green algae
  Correa Galvis, Viviana Andrea
  
• (2015) The Transcriptomic Blueprint of C4 Photosynthesis
  Külahoglu, Canan
  
• (2016) C4 photosynthesis evolution: the conditional Mt. Fuji. Curr Opin Plant Biol. Jun;31:149-54
  Heckmann D
  (See online at https://doi.org/10.1016/j.pbi.2016.04.008)
• (2016) Combining genetic and evolutionary engineering to establish C4 metabolism in C3 plants. J Exp Bot. 68(2):117-125
  Li Y, Heckmann D, Lercher MJ, Maurino VG
  (See online at https://doi.org/10.1093/jxb/erw333)
• (2016) Dissecting Long-Term Adjustments of Photoprotective and Photo-Oxidative Stress Acclimation Occurring in Dynamic Light Environments. Front Plant Sci 7:1690 eCollection2016
  Matsubara S, Schneider T, Maurino VG
  (See online at https://doi.org/10.3389/fpls.2016.01690)
• (2016) Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Curr Genet. 62(2):243-54
  Langner T, Göhre V
  (See online at https://doi.org/10.1007/s00294-015-0530-x)
• (2016) Genetic Manipulation of the Plant Pathogen Ustilago maydis to Study Fungal Biology and Plant Microbe Interactions. J Vis Exp. Sep 30;(115)
  Bösch K, Frantzeskakis L, Vraneš M, Kämper J, Schipper K, Göhre V
  (See online at https://dx.doi.org/10.3791/54522)
• (2016) Improved Metabolic Models for E. coli and Mycoplasma genitalium from GlobalFit, an Algorithm That Simultaneously Matches Growth and Non-Growth Data Sets. PLoS Comput Biol Aug 2;12(8)e1005036 eCollection 2016
  Hartleb D, Jarre F, Lercher MJ
  (See online at https://doi.org/10.1371/journal.pcbi.1005036)
• (2016) Peptides interfering with protein-protein interactions in the ethylene signaling pathway delay tomato fruit ripening. Sci Rep Aug 1;6:30634
  Bisson MM, Kessenbrock M, Müller L, Hofmann A, Schmitz F, Cristescu SM, Groth G
  (See online at https://doi.org/10.1038/srep30634)
• (2016) Photosystem II Subunit PsbS Is Involved in the Induction of LHCSR Protein-dependent Energy Dissipation in Chlamydomonas reinhardtii. J Biol Chem. Aug 12;291(33):17478-87
  Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB, Wakao S, Niyogi KK, Jahns P
  (See online at https://doi.org/10.1074/jbc.m116.737312)
• (2016) Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways. Plant Cell 28(1):102-29
  Bernsdorff F, Döhring AC, Gruner K, Schuck S, Bräutigam A, Zeier J
  (See online at https://doi.org/10.1105/tpc.15.00496)
• (2016) PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nat Plants. Feb 1;2:15225
  Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB, Wakao S, Niyogi KK, Jahns P
  (See online at https://doi.org/10.1038/nplants.2015.225)
• (2016) Regulatory and Functional Aspects of Indolic Metabolism in Plant Systemic Acquired Resistance. Mol Plant 9(5):662-81
  Stahl E, Bellwon P, Huber S, Schlaeppi K, Bernsdorff F, Vallat-Michel A, Mauch F, Zeier J
  (See online at https://doi.org/10.1016/j.molp.2016.01.005)
• (2016) Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiol 170(1):102–22
  Brilhaus D, Bräutigam A, Mettler-Altmann T, Winter K, Weber APM
  (See online at https://doi.org/10.1104/pp.15.01076)
• (2016) The genome of the fungal plant pathogen Thecaphora thlaspeos
  Franzeskakis, Lamprinos
  
• (2016) The Peroxisomal NAD Carrier from Arabidopsis Imports NAD in Exchange with AMP. Plant Physiol. Jul;171(3):2127-39
  van Roermund CW, Schroers MG, Wiese J, Facchinelli F, Kurz S, Wilkinson S, Charton L, Wanders RJ, Waterham HR, Weber AP, Linka N
  (See online at https://doi.org/10.1104/pp.16.00540)
• (2016) Transcriptional adaptation in response to changing environments in plants with specialized photosynthesis types
  Brilhaus, Dominik
  
• (2016) Understanding metabolite transport and metabolism in C4 plants through RNA-seq. Curr Opin Plant Biol 31:83-90
  Schlüter U, Denton AK, Bräutigam A3
  (See online at https://doi.org/10.1016/j.pbi.2016.03.007)
• (2017) Analysis of Peroxisomal β- Oxidation During Storage Oil Mobilization in Arabidopsis thaliana Seedlings. Methods Mol Biol. 1595:291-304
  Hielscher B, Charton L, Mettler-Altmann T, Linka N
  (See online at https://doi.org/10.1007/978-1-4939-6937-1_27)
• (2017) Biochemical Principles and Functional Aspects of Pipecolic Acid Biosynthesis in Plant Immunity. Plant Physiol. 174(1):124- 153
  Hartmann M, Kim D, Bernsdorff F, Ajami-Rashidi Z, Scholten N, Schreiber S, Zeier T, Schuck S, Reichel-Deland V, Zeier J
  (See online at https://doi.org/10.1104/pp.17.00222)
• (2017) BLISTER Regulates Polycomb-Target Genes, Represses Stress-Regulated Genes and Promotes Stress Responses in Arabidopsis thaliana Front Plant Sci.; 8:1530
  Kleinmanns JA, Schatlowski N, Heckmann D and Schubert D
  (See online at https://doi.org/10.3389/fpls.2017.01530)
• (2017) Erroneous energy-generating cycles in published genome scale metabolic networks: Identification and removal. PLoS Comput Biol. 13(4):e1005494
  Fritzemeier CJ, Hartleb D, Szappanos B, Papp B, Lercher MJ
  (See online at https://doi.org/10.1371/journal.pcbi.1005494)
• (2017) Freeze-quenched maize mesophyll and bundle sheath separation uncovers bias in previous tissue-specific RNA-Seq data. J Exp Bot. 68(2):147-160
  Denton AK, Maß J, Külahoglu C, Lercher MJ, Bräutigam A, Weber AP
  (See online at https://doi.org/10.1093/jxb/erw463)
• (2017) Hybridization and Wild Tomato
  Beddows, Thomas Ian
  
• (2017) In Vitro Analysis of Metabolite Transport Proteins. Methods Mol Biol. 1653:83-96
  Roell MS, Kuhnert F, Zamani-Nour S, Weber APM
  (See online at https://doi.org/10.1007/978-1-4939-7225-8_6)
• (2017) Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify. New Phytol. 217(1):453-466
  Dijkhuizen LW, Brouwer P, Bolhuis H, Reichart GJ, Koppers N, Huettel B, Bolger AM, Li FW, Cheng S, Liu X, Wong GK, Pryer K, Weber A, Bräutigam A, Schluepmann H
  (See online at https://doi.org/10.1111/nph.14843)
• (2017) Machine Learning Techniques for Predicting Crop Photosynthetic Capacity from Leaf Reflectance Spectra. Mol Plant. 10(6):878-890
  Heckmann D, Schlüter U, Weber APM
  (See online at https://doi.org/10.1016/j.molp.2017.04.009)
• (2017) Population genomics in wild tomatoes - the interplay of divergence and admixture. Genome Biol Evol. 9(11)3023- 3038
  Beddows I, Reddy A, Kloesges T, Rose LE
  (See online at https://doi.org/10.1093/gbe/evx224)
• (2017) The plant-dependent life cycle of Thecaphora thlaspeos: a smut fungus adapted to Brassicacea. Mol Plant Microbe Interact. 30(4):271-282
  Frantzeskakis L, Courville KJ, Pluecker L, Kellner R, Kruse J, Brachmann A, Feldbrügge M and Göhre V
  (See online at https://doi.org/10.1094/mpmi-08-16-0164-r)
• (2018) A BAHD neofunctionalization promotes tetrahydroxycinnamoyl spermine accumulation in pollen coat of the Asteraceae family. J Exp Bot. 2018 Aug 31
  Delporte M, Bernard G, Legrand G, Hielscher B, Lanoue A, Molinié R, Rambaud C, Mathiron D, Besseau S, Linka N, Hilbert JL, Gagneul D
  (See online at https://doi.org/10.1093/jxb/ery320)
• (2018) Automated high-quality reconstruction of metabolic networks from high-throughput data
  Hartleb D, Fritzemeier CJ, Lercher MJ
  (See online at https://doi.org/10.1101/282251)
• (2018) Biochemische Charakterisierung der Komponenten des ERECTA-Signalwegs
  Hofmann, Alexander
  
• (2018) Broadspectrum inhibition of Phytophthora infestans by fungal endophytes. FEMS Microbiol Ecol. 94(4)
  de Vries S, von Dahlen JK, Schnake A, Ginschel S, Schulz B, Rose LE
  (See online at https://doi.org/10.1093/femsec/fiy037)
• (2018) Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance. Proc Biol Sci 285(1873)
  de Vries S, Kukuk A, von Dahlen JK, Schnake A, Kloesges T, Rose LE
  (See online at https://doi.org/10.1098/rspb.2017.2560)
• (2018) Factors determining hybridization rate in plants: A case study in Michigan. Perspectives in Plant Ecology, Evolution and Systematics 34(2018)51-60
  Beddows I, Rose LE
  (See online at https://doi.org/10.1016/j.ppees.2018.07.003)
• (2018) Fine-Tuning of Photosynthesis Requires CURVATURE THYLAKOID1-Mediated Thylakoid Plasticit 176(3)2351-2364
  Pribil M, Sandoval-Ibáñez O, Xu W, Sharma A, Labs M, Liu Q, Galgenmüller C, Schneider T, Wessels M, Matsubara S, Jansson S, Wanner G, Leister D
  (See online at https://doi.org/10.1104/pp.17.00863)
• (2018) Flavin Monooxygenase- Generated N-Hydroxypipecolic Acid Is a Critical Element of Plant Systemic Immunity. Cell 173(2):456-469
  Hartmann M, Zeier T, Bernsdorff F, Reichel-Deland V, Kim D, Hohmann M, Scholten N, Schuck S, Bräutigam A, Hölzel T, Ganter C, Zeier J
  (See online at https://doi.org/10.1016/j.cell.2018.02.049)
• (2018) Mathematical Modeling and Evolutionary Analyses of Cell-Surface Signaling in Plants
  Richards, Sarah Rose
  
• (2018) Modeling Cellular Resource Allocation Reveals Low Phenotypic Plasticity of C4 Plants and Infers Environments of C4 Photosynthesis Evolution
  Sundermann E, Lercher MJ, Heckmann D
  (See online at https://doi.org/10.1101/371096)
• (2018) On plant defense signaling networks and early land plant evolution. Commun Integr Biol. 9;11(3):1-14
  de Vries S, de Vries J, von Dahlen JK, Gould SB, Archibald JM, Rose LE, Slamovits CH
  (See online at https://doi.org/10.1080/19420889.2018.1486168)
• (2018) Rapid evolution in the tug-of-war between microbes and plants. New Phytol. 2018 Jul;219(1):12-14
  Frantzeskakis L, von Dahlen JK, Panstruga R, Rose LE
  (See online at https://doi.org/10.1111/nph.15220)
• (2018) Reporter-based forward genetic screen to identify bundle sheath anatomy mutants in A. thaliana. Plant J.
  Döring F, Billakurthi K, Gowik U, Sultmanis S, Khoshravesh R, Das Gupta S, Sage TL, Westhoff P
  (See online at https://doi.org/10.1111/tpj.14165)
• (2018) The germinal centre kinase Don3 is essential for unconventional secretion of chitinase Cts1 in Ustilago maydis. Biochim Biophys Acta Proteins Proteom. pii: S1570-9639(18)30176-6
  Aschenbroich J, Hußnätter K, Stoffels, T. Langner T, Zander S, Sandrock B, Bölker M, Feldbrügge M and Schipper K
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