Auxin boosts energy generation pathways to fuel pollen maturation in barley

Current Biology - Tập 32 - Trang 1798-1811.e8 - 2022
Dhika Amanda1, Felix P. Frey1, Ulla Neumann1, Marine Przybyl1, Jan Šimura2, Youjun Zhang3,4, Zongliang Chen5, Andrea Gallavotti5,6, Alisdair R. Fernie3,4, Karin Ljung2, Iván F. Acosta1
1Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany
2Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden
3Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany;
4Center of Plant Systems Biology and Biotechnology, 4000, Plovdiv, Bulgaria
5Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ 08854, USA
6Department of Plant Biology, Rutgers University, New Brunswick, NJ, 08901, USA

Tài liệu tham khảo

Christensen, 1972, Pollen wall and tapetalorbicularwalldevelopment in Sorghum bicolor (Gramineae), Am.J.Bot., 59, 43, 10.1002/j.1537-2197.1972.tb10061.x Rutley, 2015, A decade of pollen transcriptomics, Plant Reprod., 28, 73, 10.1007/s00497-015-0261-7 Zhang, 2010, Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development, Plant Cell, 22, 672, 10.1105/tpc.109.073668 Adamczyk, 2009, MIKC∗ MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis, Plant Physiol., 149, 1713, 10.1104/pp.109.135806 Liu, 2013, Functional conservation of MIKC∗-Type MADS box genes in Arabidopsis and rice pollen maturation, Plant Cell, 25, 1288, 10.1105/tpc.113.110049 Verelst, 2007, MADS-complexes regulate transcriptome dynamics during pollen maturation, Genome Biol., 8, R249, 10.1186/gb-2007-8-11-r249 McConn, 1996, The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant, Plant Cell, 8, 403, 10.2307/3870321 Mandaokar, 2006, Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling, Plant J., 46, 984, 10.1111/j.1365-313X.2006.02756.x Cheng, 2006, Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis, Genes Dev., 20, 1790, 10.1101/gad.1415106 Yao, 2018, Auxin production in diploid microsporocytes is necessary and sufficient for early stages of pollen development, PLoS Genet., 14, e1007397, 10.1371/journal.pgen.1007397 Nagpal, 2005, Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation, Development, 132, 4107, 10.1242/dev.01955 Ru, 2006, Plant fertility defects induced by the enhanced expression of microRNA167, Cell Res., 16, 457, 10.1038/sj.cr.7310057 Cecchetti, 2013, Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis, Plant J., 74, 411, 10.1111/tpj.12130 Cecchetti, 2008, Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation, Plant Cell, 20, 1760, 10.1105/tpc.107.057570 Cecchetti, 2004, Expression of rolB in tobacco flowers affects the coordinated processes of anther dehiscence and style elongation, Plant J., 38, 512, 10.1111/j.0960-7412.2004.02064.x Hirano, 2008, Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice, Plant Cell Physiol., 49, 1429, 10.1093/pcp/pcn123 Song, 2018, OsFTIP7 determines auxin-mediated anther dehiscence in rice, Nat. Plants, 4, 495, 10.1038/s41477-018-0175-0 Zhao, 2013, A role for a dioxygenase in auxin metabolism and reproductive development in rice, Dev. Cell, 27, 113, 10.1016/j.devcel.2013.09.005 Clément, 2001, Anther plastids in angiosperms, Bot.Rev., 67, 54, 10.1007/BF02857849 Pacini, 1992, Development of plastids in pollen and tapetum of rye-grass, Lolium perenne L., Ann.Bot., 70, 179, 10.1093/oxfordjournals.aob.a088455 Lee, 2016, Plastidic phosphoglucomutase and ADP-glucose pyrophosphorylase mutants impair starch synthesis in rice pollen grains and cause male sterility, J.Exp.Bot., 67, 5557, 10.1093/jxb/erw324 Geigenberger, 2011, Regulation of starch biosynthesis in response to a fluctuating environment, Plant Physiol., 155, 1566, 10.1104/pp.110.170399 Geigenberger, 2004, Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers, PlantCellEnviron., 27, 655 Dickinson, 1965, Germination of lilypollen: respiration and tubegrowth, Science, 150, 1818, 10.1126/science.150.3705.1818 Dickinson, 1966, Inhibition of pollenrespiration by oligomycin, Nature, 210, 1362, 10.1038/2101362a0 Dickinson, 1968, Rapid starch synthesis associated with increased respiration in germinating lily pollen, Plant Physiol., 43, 1, 10.1104/pp.43.1.1 Franckowiak, 2012, Descriptions of barleygeneticstocks for 2012, Barley Genet.Newsl., 42, 36 Druka, 2011, Genetic dissection of barley morphology and development, Plant Physiol., 155, 617, 10.1104/pp.110.166249 Waddington, 1983, A quantitativescale of spikeinitial and pistildevelopment in barley and wheat, Ann.Bot., 51, 119, 10.1093/oxfordjournals.aob.a086434 Matsui, 2000, Rapid swelling of pollengrains in the dehiscinganther of two-rowed barley (Hordeum distichum L. emend. Lam.), Ann.Bot., 85, 345, 10.1006/anbo.1999.1051 Rehman, 2004, Does barley (Hordeum vulgare L.) pollen swell in fractions of a second?, Plant Sci., 167, 137, 10.1016/j.plantsci.2004.03.013 Mashiguchi, 2011, The main auxin biosynthesis pathway in Arabidopsis, Proc.Natl.Acad.Sci. USA, 108, 18512, 10.1073/pnas.1108434108 Won, 2011, Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis, Proc.Natl.Acad.Sci. USA, 108, 18518, 10.1073/pnas.1108436108 Sieber, 2017, The role of metabolic states in development and disease, Curr.Opin.Genet.Dev., 45, 58, 10.1016/j.gde.2017.03.002 Tennessen, 2011, The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth, Cell Metab., 13, 139, 10.1016/j.cmet.2011.01.005 Verbist, 2016, Metabolic maintenance of cell asymmetry following division in activated T lymphocytes, Nature, 532, 389, 10.1038/nature17442 Fu, 2021, The TOR-EIN2 axis mediates nuclear signalling to modulate plant growth, Nature, 591, 288, 10.1038/s41586-021-03310-y Li, 2018, Modulating plant growth-metabolism coordination for sustainable agriculture, Nature, 560, 595, 10.1038/s41586-018-0415-5 Rolletschek, 2004, Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains, J.Exp.Bot., 55, 1351, 10.1093/jxb/erh130 Bernardi, 2019, Transcriptomic and metabolomic analysis of ZmYUC1 mutant reveals the role of auxin during early endosperm formation in maize, Plant Sci., 281, 133, 10.1016/j.plantsci.2019.01.027 McAdam, 2017, Evidence that auxin is required for normal seed size and starch synthesis in pea, New Phytol., 216, 193, 10.1111/nph.14690 Commoner, 1941, On the relation between growth and respiration in the Avenacoleoptile, J.Gen.Physiol., 24, 279, 10.1085/jgp.24.3.279 Leonova, 1985, Promotion of respiration by auxin in the induction of cell division in suspension culture, J.Plant Growth Regul., 4, 169, 10.1007/BF02266954 Batista-Silva, 2019, Modulation of auxin signalling through DIAGETROPICA and ENTIRE differentially affects tomato plant growth via changes in photosynthetic and mitochondrial metabolism, Plant Cell Environ., 42, 448, 10.1111/pce.13413 Mair, 2015, SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants, eLife, 4, 10.7554/eLife.05828 Nukarinen, 2016, Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation, Sci.Rep., 6, 31697, 10.1038/srep31697 Krouk, 2011, A framework integrating plant growth with hormones and nutrients, Trends Plant Sci., 16, 178, 10.1016/j.tplants.2011.02.004 Zhang, 2001, Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley, Plant J., 28, 431, 10.1046/j.1365-313X.2001.01167.x Kuang, 1996, Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation in Arabidopsis thaliana, Protoplasma, 194, 81, 10.1007/BF01273170 Brumos, 2018, Local auxinbiosynthesisis a keyregulator of plantdevelopment, Dev. Cell, 47, 306, 10.1016/j.devcel.2018.09.022 Cecchetti, 2017, An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis, New Phytol., 213, 1194, 10.1111/nph.14207 Franckowiak, 1988, Identification of three new loci which control male sterility of barley, Barley Genet.Newsl., 18, 11 Hockett, 1984, Identification of three new loci which control male sterility of barley, Barley Genet.Newsl., 14, 70 Wilson, 2012, Preparation of plant cells for transmission electron microscopy to optimize immunogold labeling of carbohydrate and protein epitopes, Nat.Protoc., 7, 1716, 10.1038/nprot.2012.096 Peterson, 2010, A simplified method for differential staining of aborted and non-aborted pollen grains, Int.J.Plant Biol., 1, e13, 10.4081/pb.2010.e13 Alexander, 1969, Differential staining of aborted and nonaborted pollen, Stain Technol., 44, 117, 10.3109/10520296909063335 Aloni, 2001, The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination, Physiol. Plant, 112, 505, 10.1034/j.1399-3054.2001.1120407.x Liu, 2011, Distribution of starch and neutral lipids in the developing anthers of Ipomoea cairica, Ann.Bot.Fenn., 48, 256, 10.5735/085.048.0306 Wang, 2019, Cytological and proteomicanalysis of wheatpollenabortioninduced by chemicalhybridizationagent, Int.J.Mol.Sci., 20 Gomori, 1952 Mascher, 2017, A chromosome conformation capture ordered sequence of the barley genome, Nature, 544, 427, 10.1038/nature22043 Monat, 2019, TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools, Genome Biol., 20, 284, 10.1186/s13059-019-1899-5 Gol, 2021, Ppd-H1 integrates drought stress signals to control spike development and flowering time in barley, J.Exp.Bot., 72, 122, 10.1093/jxb/eraa261 Lawrenson, 2015, Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease, Genome Biol., 16, 258, 10.1186/s13059-015-0826-7 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Li, 2011, A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data, Bioinformatics, 27, 2987, 10.1093/bioinformatics/btr509 McKenna, 2010, The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 20, 1297, 10.1101/gr.107524.110 Danecek, 2011, The variant call format and VCFtools, Bioinformatics, 27, 2156, 10.1093/bioinformatics/btr330 Kumar, 2018, MEGA X: molecular evolutionarygeneticsanalysis across computingplatforms, Mol.Biol.Evol., 35, 1547, 10.1093/molbev/msy096 Ronquist, 2012, MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space, Syst.Biol., 61, 539, 10.1093/sysbio/sys029 Ruijter, 2009, Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data, Nucleic Acids Res., 37, e45, 10.1093/nar/gkp045 Patro, 2017, Salmon provides fast and bias-aware quantification of transcript expression, Nat. Methods, 14, 417, 10.1038/nmeth.4197 Mejía-Guerra, 2019, A k-mer grammar analysis to uncover maize regulatory architecture, BMC Plant Biol., 19, 103, 10.1186/s12870-019-1693-2 Mori, 2006, GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization, Nat. Cell Biol., 8, 64, 10.1038/ncb1345 Liu, 2016, Receptor-likekinase RUPO interacts with potassiumtransporters to regulatepollentubegrowth and integrity in rice, PLOS Genet., 12, e1006085, 10.1371/journal.pgen.1006085 Micali, 2011, Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria, Cell.Microbiol., 13, 210, 10.1111/j.1462-5822.2010.01530.x Phillips, 2015, The effect of temperature on the male and female recombination landscape of barley, New Phytol., 208, 421, 10.1111/nph.13548 Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 32, 1792, 10.1093/nar/gkh340 Jöst, 2016, The INDETERMINATE DOMAIN protein BROAD LEAF1 limitsbarleyleafwidth by restrictinglateralproliferation, Curr.Biol., 26, 903, 10.1016/j.cub.2016.01.047 Hensel, 2009, Agrobacterium-mediated gene transfer to cereal crop plants: current protocols for barley, wheat, triticale, and maize, Int.J. Plant Genomics, 2009, 835608, 10.1155/2009/835608 Novák, 2012, Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome, Plant J., 72, 523, 10.1111/j.1365-313X.2012.05085.x Oñate-Sánchez, 2008, DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques, BMC Res. Notes, 1, 93, 10.1186/1756-0500-1-93 Jackson, 1992, In situ hybridization in plants, 1, 163 Bortiri, 2006, ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize, Plant Cell, 18, 574, 10.1105/tpc.105.039032 Chauvin, 2013, Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals, New Phytol., 197, 566, 10.1111/nph.12029 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Ritchie, 2015, limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007 Zhong, 2021, INTERMEDIUM-M encodes an HvAP2L-H5 ortholog and is required for inflorescence indeterminacy and spikelet determinacy in barley, Proc.Natl.Acad.Sci. USA, 118, 10.1073/pnas.2011779118 Alexa, 2006, Improved scoring of functional groups from gene expression data by decorrelating GO graph structure, Bioinformatics, 22, 1600, 10.1093/bioinformatics/btl140 Hedhly, 2016, Starch turnover and metabolism during flower and earlyembryodevelopment, Plant Physiol., 172, 2388, 10.1104/pp.16.00916 Schwacke, 2003, ARAMEMNON, a novel database for Arabidopsis integral membrane proteins, Plant Physiol., 131, 16, 10.1104/pp.011577 Elbourne, 2017, TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life, Nucleic Acids Res., 45, D320, 10.1093/nar/gkw1068 Michard, 2017, Signaling with ions: thekeystone for apicalcellgrowth and morphogenesis in pollentubes, Plant Physiol., 173, 91, 10.1104/pp.16.01561 Galli, 2018, The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family, Nat.Commun., 9, 4526, 10.1038/s41467-018-06977-6 Tu, 2020, Reconstructing the maize leaf regulatory network using ChIP-seq data of 104 transcription factors, Nat.Commun., 11, 5089, 10.1038/s41467-020-18832-8 Lisec, 2006, Gas chromatography mass spectrometry-based metabolite profiling in plants, Nat.Protoc., 1, 387, 10.1038/nprot.2006.59 Kopka, 2005, GMD@CSB. DB: the Golm metabolome database, Bioinformatics, 21, 1635, 10.1093/bioinformatics/bti236 Rosado-Souza, 2019, Cassava metabolomics and starch quality, Curr.Protoc.PlantBiol., 4, e20102, 10.1002/cppb.20102