دورية أكاديمية
Strong prevalence of light regime-specific QTL in Arabidopsis detected using automated high-throughput phenotyping in fluctuating or constant light.
العنوان: | Strong prevalence of light regime-specific QTL in Arabidopsis detected using automated high-throughput phenotyping in fluctuating or constant light. |
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المؤلفون: | Heuermann MC; Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany., Meyer RC; Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany., Knoch D; Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany., Tschiersch H; Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany., Altmann T; Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany. |
المصدر: | Physiologia plantarum [Physiol Plant] 2024 Mar-Apr; Vol. 176 (2), pp. e14255. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Scandinavian Society For Plant Physiology Country of Publication: Denmark NLM ID: 1256322 Publication Model: Print Cited Medium: Internet ISSN: 1399-3054 (Electronic) Linking ISSN: 00319317 NLM ISO Abbreviation: Physiol Plant Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Copenhagen : Scandinavian Society For Plant Physiology Original Publication: Lund, Sweden [etc.] |
مواضيع طبية MeSH: | Arabidopsis*/physiology , Arabidopsis Proteins*/metabolism, Prevalence ; Photosynthesis/genetics ; Phenotype |
مستخلص: | Plants have evolved and adapted under dynamic environmental conditions, particularly to fluctuating light, but plant research has often focused on constant growth conditions. To quantitatively asses the adaptation to fluctuating light, a panel of 384 natural Arabidopsis thaliana accessions was analyzed in two parallel independent experiments under fluctuating and constant light conditions in an automated high-throughput phenotyping system upgraded with supplemental LEDs. While the integrated daily photosynthetically active radiation was the same under both light regimes, plants in fluctuating light conditions accumulated significantly less biomass and had lower leaf area during their measured vegetative growth than plants in constant light. A total of 282 image-derived architectural and/or color-related traits at six common time points, and 77 photosynthesis-related traits from one common time point were used to assess their associations with genome-wide natural variation for both light regimes. Out of the 3000 significant marker-trait associations (MTAs) detected, only 183 (6.1%) were common for fluctuating and constant light conditions. The prevalence of light regime-specific QTL indicates a complex adaptation. Genes in linkage disequilibrium with fluctuating light-specific MTAs with an adjusted repeatability value >0.5 were filtered for gene ontology terms containing "photo" or "light", yielding 15 selected candidates. The candidate genes are involved in photoprotection, PSII maintenance and repair, maintenance of linear electron flow, photorespiration, phytochrome signaling, and cell wall expansion, providing a promising starting point for further investigations into the response of Arabidopsis thaliana to fluctuating light conditions. (© 2024 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.) |
References: | Akmakjian, G.Z., Riaz, N. and Guerinot, M.L. (2021) Photoprotection during iron deficiency is mediated by the bHLH transcription factors PYE and ILR3. Proc. Natl. Acad. Sci. U.S.A., 118, e2024918118. Alexa, A. and Rahnenfuhrer, J. (2016) topGO: Enrichment Analysis for Gene Ontology. Alonso‐Blanco, C., Andrade, J., Becker, C., et al. (2016) 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell, 166, 481–491. Arend, D., Lange, M., Chen, J., Colmsee, C., Flemming, S., Hecht, D. and Scholz, U. (2014) e!DAL ‐ a framework to store, share and publish research data. BMC Bioinformatics, 15, 214. Barr, D.J., Levy, R., Scheepers, C. and Tily, H.J. (2013) Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68. Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015) Fitting Linear Mixed‐Effects Models Using lme4, https://github.com/lme4/lme4/. Journal of Statistical Software, 67. Bricker, T.M., Roose, J.L., Zhang, P. and Frankel, L.K. (2013) The PsbP family of proteins. Photosynthesis Research, 116, 235–250. Chen, C.‐Y., Ho, S.‐S., Kuo, T.‐Y., Hsieh, H.‐L. and Cheng, Y.‐S. (2017) Structural basis of jasmonate‐amido synthetase FIN219 in complex with glutathione S‐transferase FIP1 during the JA signal regulation. Proc Natl Acad Sci U S A, 114, E1815–E1824. Chen, H.‐J., Chen, C.‐L. and Hsieh, H.‐L. (2015) Far‐Red Light‐Mediated Seedling Development in Arabidopsis Involves FAR‐RED INSENSITIVE 219/JASMONATE RESISTANT 1‐Dependent and ‐Independent Pathways. PLoS ONE, 10, e0132723. Cheng, C.‐Y., Krishnakumar, V., Chan, A.P., Thibaud‐Nissen, F., Schobel, S. and Town, C.D. (2017) Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. The Plant Journal, 89, 789–804. De Souza, A.P., Burgess, S.J., Doran, L., et al. (2022) Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science, 377, 851–854. Dornbusch, T., Michaud, O., Xenarios, I. and Fankhauser, C. (2014) Differentially phased leaf growth and movements in Arabidopsis depend on coordinated circadian and light regulation. Plant Cell, 26, 3911–3921. Durand, M., Matule, B., Burgess, A.J. and Robson, T.M. (2021) Sunfleck properties from time series of fluctuating light. Agricultural and Forest Meteorology, 308–309, 108554. Emiliani, J., Grotewold, E., Falcone Ferreyra, M.L. and Casati, P. (2013) Flavonols Protect Arabidopsis Plants against UV‐B Deleterious Effects. Molecular Plant, 6, 1376–1379. Esmon, C.A., Tinsley, A.G., Ljung, K., Sandberg, G., Hearne, L.B. and Liscum, E. (2006) A gradient of auxin and auxin‐dependent transcription precedes tropic growth responses. Proc. Natl. Acad. Sci. U.S.A., 103, 236–241. Filiault, D.L. and Maloof, J.N. (2012) A genome‐wide association study identifies variants underlying the Arabidopsis thaliana shade avoidance response. PLoS Genet., 8, e1002589. Filo, J., Wu, A., Eliason, E., Richardson, T., Thines, B.C. and Harmon, F.G. (2015) Gibberellin driven growth in elf3 mutants requires PIF4 and PIF5. Plant Signal Behav, 10, e992707. Friml, J., Wiśniewska, J., Benková, E., Mendgen, K. and Palme, K. (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature, 415, 806–809. Garcia‐Molina, A. and Leister, D. (2020) Accelerated relaxation of photoprotection impairs biomass accumulation in Arabidopsis. Nat. Plants, 6, 9–12. Gelderen, K. van, Kang, C., Paalman, R., Keuskamp, D., Hayes, S. and Pierik, R. (2018) Far‐Red Light Detection in the Shoot Regulates Lateral Root Development through the HY5 Transcription Factor. Plant Cell, 30, 101–116. Hartmann, U., Sagasser, M., Mehrtens, F., Stracke, R. and Weisshaar, B. (2005) Differential combinatorial interactions of cis‐acting elements recognized by R2R3‐MYB, BZIP, and BHLH factors control light‐responsive and tissue‐specific activation of phenylpropanoid biosynthesis genes. Plant Mol. Biol., 57, 155–171. Hogewoning, S.W., Douwstra, P., Trouwborst, G., Ieperen, W. van and Harbinson, J. (2010) An artificial solar spectrum substantially alters plant development compared with usual climate room irradiance spectra. Journal of Experimental Botany, 61, 1267–1276. Holalu, S.V., Reddy, S.K., Blackman, B.K. and Finlayson, S.A. (2020) Phytochrome interacting factors 4 and 5 regulate axillary branching via bud abscisic acid and stem auxin signalling. Plant Cell Environ, 43, 2224–2238. Hornitschek, P., Kohnen, M.V., Lorrain, S., et al. (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. The Plant Journal, 71, 699–711. Hsieh, H.L., Okamoto, H., Wang, M., Ang, L.H., Matsui, M., Goodman, H. and Deng, X.W. (2000) FIN219, an auxin‐regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev., 14, 1958–1970. Hu, W., Franklin, K.A., Sharrock, R.A., Jones, M.A., Harmer, S.L. and Lagarias, J.C. (2013) Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis. Proc. Natl. Acad. Sci. U.S.A., 110, 1542–1547. Huang, W., Cai, Y.‐F., Wang, J.‐H. and Zhang, S.‐B. (2018) Chloroplastic ATP synthase plays an important role in the regulation of proton motive force in fluctuating light. Journal of Plant Physiology, 226, 40–47. Huang, W., Hu, H. and Zhang, S.‐B. (2015) Photorespiration plays an important role in the regulation of photosynthetic electron flow under fluctuating light in tobacco plants grown under full sunlight. Front. Plant Sci., 6. Available at: http://journal.frontiersin.org/Article/10.3389/fpls.2015.00621/abstract. Ingvarsson, P.K. and Street, N.R. (2011) Association genetics of complex traits in plants: Tansley review. New Phytologist, 189, 909–922. Junker, A., Muraya, M.M., Weigelt‐Fischer, K., Arana‐Ceballos, F., Klukas, C., Melchinger, A.E., Meyer, R.C., Riewe, D. and Altmann, T. (2015) Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems. Front Plant Sci, 5. Jurić, S., Hazler‐Pilepić, K., Tomasić, A., et al. (2009) Tethering of ferredoxin:NADP+ oxidoreductase to thylakoid membranes is mediated by novel chloroplast protein TROL. The Plant Journal, 60, 783–794. Kaiser, E., Morales, A. and Harbinson, J. (2018) Fluctuating Light Takes Crop Photosynthesis on a Rollercoaster Ride. Plant Physiol., 176, 977–989. Keuskamp, D.H., Pollmann, S., Voesenek, L.A.C.J., Peeters, A.J.M. and Pierik, R. (2010) Auxin transport through PIN‐FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc. Natl. Acad. Sci. U.S.A., 107, 22740–22744. Khanna, R., Shen, Y., Marion, C.M., Tsuchisaka, A., Theologis, A., Schäfer, E. and Quail, P.H. (2007) The basic helix‐loop‐helix transcription factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell, 19, 3915–3929. Klukas, C., Chen, D. and Pape, J.‐M. (2014) Integrated Analysis Platform: An Open‐Source Information System for High‐Throughput Plant Phenotyping. Plant Physiol., 165, 506–518. Knoch, D., Abbadi, A., Grandke, F., Meyer, R.C., Samans, B., Werner, C.R., Snowdon, R.J. and Altmann, T. (2019) Strong temporal dynamics of QTL action on plant growth progression revealed through high‐throughput phenotyping in canola. Plant Biotechnology Journal, pbi.13171. Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K. and Long, S.P. (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354, 857–861. Kulheim, C., Agren, J. and Jansson, S. (2002) Rapid Regulation of Light Harvesting and Plant Fitness in the Field. Science, 297, 91–93. Lamesch, P., Berardini, T.Z., Li, D., et al. (2011) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research, 40, D1202–D1210. Langstroff, A., Heuermann, M.C., Stahl, A. and Junker, A. (2022) Opportunities and limits of controlled‐environment plant phenotyping for climate response traits. Theor Appl Genet, 135, 1–16. Lehretz, G.G., Schneider, A., Leister, D. and Sonnewald, U. (2022) High non‐photochemical quenching of VPZ transgenic potato plants limits CO 2 assimilation under high light conditions and reduces tuber yield under fluctuating light. JIPB, 64, 1821–1832. Lichtenthaler, H.K., Babani, F. and Langsdorf, G. (2007) Chlorophyll fluorescence imaging of photosynthetic activity in sun and shade leaves of trees. Photosynthesis Research, 93, 235–244. Liu, X., Huang, M., Fan, B., Buckler, E.S. and Zhang, Z. (2016) Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome‐Wide Association Studies. PLoS Genet., 12, e1005767. Long, S.P., Taylor, S.H., Burgess, S.J., Carmo‐Silva, E., Lawson, T., De Souza, A.P., Leonelli, L. and Wang, Y. (2022) Into the Shadows and Back into Sunlight: Photosynthesis in Fluctuating Light. Annu. Rev. Plant Biol., 73, 617–648. Long, T.A., Tsukagoshi, H., Busch, W., Lahner, B., Salt, D.E. and Benfey, P.N. (2010) The bHLH Transcription Factor POPEYE Regulates Response to Iron Deficiency in Arabidopsis Roots. The Plant Cell, 22, 2219–2236. Lu, Y., Hall, D.A. and Last, R.L. (2011) A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell, 23, 1861–1875. Lutziger, I. and Oliver, D.J. (2001) Characterization of Two cDNAs Encoding Mitochondrial Lipoamide Dehydrogenase from Arabidopsis. Plant Physiology, 127, 615–623. Maiwald, D., Dietzmann, A., Jahns, P., Pesaresi, P., Joliot, P., Joliot, A., Levin, J.Z., Salamini, F. and Leister, D. (2003) Knock‐Out of the Genes Coding for the Rieske Protein and the ATP‐Synthase δ‐Subunit of Arabidopsis. Effects on Photosynthesis, Thylakoid Protein Composition, and Nuclear Chloroplast Gene Expression. Plant Physiology, 133, 191–202. Matsubara, S. (2018) Growing plants in fluctuating environments: why bother? Journal of Experimental Botany, 69, 4651–4654. Matuszyńska, A., Heidari, S., Jahns, P. and Ebenhöh, O. (2016) A mathematical model of non‐photochemical quenching to study short‐term light memory in plants. Biochimica et Biophysica Acta (BBA) ‐ Bioenergetics, 1857, 1860–1869. Meyer, R.C., Weigelt‐Fischer, K., Knoch, D., Heuermann, M., Zhao, Y. and Altmann, T. (2021) Temporal dynamics of QTL effects on vegetative growth in Arabidopsis thaliana Z. Wilson, ed. Journal of Experimental Botany, 72, 476–490. Moriconi, V., Binkert, M., Costigliolo, C., Sellaro, R., Ulm, R. and Casal, J.J. (2018) Perception of Sunflecks by the UV‐B Photoreceptor UV RESISTANCE LOCUS8. Plant Physiol., 177, 75–81. Mounet, F., Moing, A., Kowalczyk, M., et al. (2012) Down‐regulation of a single auxin efflux transport protein in tomato induces precocious fruit development. Journal of Experimental Botany, 63, 4901–4917. Nakagawa, S. and Schielzeth, H. (2010) Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc, 85, 935–956. Nakamura, Y., Kimura, A., Saga, H., et al. (2007) Differential metabolomics unraveling light/dark regulation of metabolic activities in Arabidopsis cell culture. Planta, 227, 57–66. Pearcy, R.W., Roden, J.S. and Gamon, J.A. (1990) Sunfleck dynamics in relation to canopy structure in a soybean (Glycine max (L.) Merr.) canopy. Agricultural and Forest Meteorology, 52, 359–372. Preuss, A., Stracke, R., Weisshaar, B., Hillebrecht, A., Matern, U. and Martens, S. (2009) Arabidopsis thaliana expresses a second functional flavonol synthase. FEBS Lett., 583, 1981–1986. R Core Team (2021) R: A Language and Environment for Statistical Computing, https://www.r-project.org. Available at: http://www.R-project.org/. Sakuraba, Y., Jeong, J., Kang, M.‐Y., Kim, J., Paek, N.‐C. and Choi, G. (2014) Phytochrome‐interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nature Communications, 5, 4636. Schneider, T., Bolger, A., Zeier, J., Preiskowski, S., Benes, V., Trenkamp, S., Usadel, B., Farré, E.M. and Matsubara, S. (2019) Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression. Plant Physiol., 179, 1632–1657. Sellaro, R., Yanovsky, M.J. and Casal, J.J. (2011) Repression of shade‐avoidance reactions by sunfleck induction of HY5 expression in Arabidopsis. The Plant Journal, 68, 919–928. Sharma, A., Sharma, B., Hayes, S., Kerner, K., Hoecker, U., Jenkins, G.I. and Franklin, K.A. (2019) UVR8 disrupts stabilisation of PIF5 by COP1 to inhibit plant stem elongation in sunlight. Nat Commun, 10, 4417. Slattery, R.A., Walker, B.J., Weber, A.P.M. and Ort, D.R. (2018) The Impacts of Fluctuating Light on Crop Performance. Plant Physiol., 176, 990–1003. Stacklies, W., Redestig, H., Scholz, M., Walther, D. and Selbig, J. (2007) pcaMethods a bioconductor package providing PCA methods for incomplete data. Bioinformatics, 23, 1164–1167. Staswick, P.E., Tiryaki, I. and Rowe, M.L. (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole‐3‐acetic acids in an assay for adenylation. Plant Cell, 14, 1405–1415. Stoffel, M.A., Nakagawa, S. and Schielzeth, H. (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed‐effects models, https://github.com/mastoffel/rptR S. Goslee, ed. Methods Ecol Evol, 8, 1639–1644. Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z., Xu, W. and Su, Z. (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research, 45, W122–W129. Timm, S., Wittmiß, M., Gamlien, S., et al. (2015) Mitochondrial Dihydrolipoyl Dehydrogenase Activity Shapes Photosynthesis and Photorespiration of Arabidopsis thaliana. Plant Cell, 27, 1968–1984. Townsend, A.J., Retkute, R., Chinnathambi, K., Randall, J.W.P., Foulkes, J., Carmo‐Silva, E. and Murchie, E.H. (2018) Suboptimal Acclimation of Photosynthesis to Light in Wheat Canopies. Plant Physiol., 176, 1233–1246. Tschiersch, H., Junker, A., Meyer, R.C. and Altmann, T. (2017) Establishment of integrated protocols for automated high throughput kinetic chlorophyll fluorescence analyses. Plant Methods, 13, 54. Ushijima, T., Hanada, K., Gotoh, E., et al. (2017) Light Controls Protein Localization through Phytochrome‐Mediated Alternative Promoter Selection. Cell, 171, 1316‐1325.e12. Vialet‐Chabrand, S., Matthews, J.S.A., Simkin, A.J., Raines, C.A. and Lawson, T. (2017) Importance of Fluctuations in Light on Plant Photosynthetic Acclimation. Plant Physiol., 173, 2163–2179. Vojta, L., Carić, D., Cesar, V., Antunović Dunić, J., Lepeduš, H., Kveder, M. and Fulgosi, H. (2015) TROL‐FNR interaction reveals alternative pathways of electron partitioning in photosynthesis. Sci Rep, 5, 10085. Wang, H. and Deng, X.W. (2002) Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. EMBO J., 21, 1339–1349. Wei, L., Guo, J., Ouyang, M., Sun, X., Ma, J., Chi, W., Lu, C. and Zhang, L. (2010) LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J. Biol. Chem., 285, 21391–21398. Yang, P., Van Der Tol, C., Campbell, P.K.E. and Middleton, E.M. (2021) Unraveling the physical and physiological basis for the solar‐ induced chlorophyll fluorescence and photosynthesis relationship using continuous leaf and canopy measurements of a corn crop. Biogeosciences, 18, 441–465. Yi, X., Hargett, S.R., Liu, H., Frankel, L.K. and Bricker, T.M. (2007) The PsbP Protein Is Required for Photosystem II Complex Assembly/Stability and Photoautotrophy in Arabidopsis thaliana. J. Biol. Chem., 282, 24833–24841. Zhang, X.‐Q., Wei, P.‐C., Xiong, Y.‐M., Yang, Y., Chen, J. and Wang, X.‐C. (2011) Overexpression of the Arabidopsis α‐expansin gene AtEXPA1 accelerates stomatal opening by decreasing the volumetric elastic modulus. Plant Cell Rep, 30, 27–36. Zhong, H., Liu, S., Meng, X., Sun, T., Deng, Y., Kong, W., Peng, Z. and Li, Y. (2021) Uncovering the genetic mechanisms regulating panicle architecture in rice with GPWAS and GWAS. BMC Genomics, 22, 86. |
معلومات مُعتمدة: | 491250510 Deutsche Forschungsgemeinschaft |
المشرفين على المادة: | 0 (Arabidopsis Proteins) |
تواريخ الأحداث: | Date Created: 20240326 Date Completed: 20240327 Latest Revision: 20240327 |
رمز التحديث: | 20240327 |
DOI: | 10.1111/ppl.14255 |
PMID: | 38528708 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1399-3054 |
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DOI: | 10.1111/ppl.14255 |