Glucose-6-P/phosphate translocator2 mediates the phosphoglucose-isomerase1-independent response to microbial volatiles

. 2022 Nov 28 ; 190 (4) : 2137-2154.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36111879

In Arabidopsis (Arabidopsis thaliana), the plastidial isoform of phosphoglucose isomerase (PGI1) mediates photosynthesis, metabolism, and development, probably due to its involvement in the synthesis of isoprenoid-derived signals in vascular tissues. Microbial volatile compounds (VCs) with molecular masses of <45 Da promote photosynthesis, growth, and starch overaccumulation in leaves through PGI1-independent mechanisms. Exposure to these compounds in leaves enhances the levels of GLUCOSE-6-PHOSPHATE/PHOSPHATE TRANSLOCATOR2 (GPT2) transcripts. We hypothesized that the PGI1-independent response to microbial volatile emissions involves GPT2 action. To test this hypothesis, we characterized the responses of wild-type (WT), GPT2-null gpt2-1, PGI1-null pgi1-2, and pgi1-2gpt2-1 plants to small fungal VCs. In addition, we characterized the responses of pgi1-2gpt2-1 plants expressing GPT2 under the control of a vascular tissue- and root tip-specific promoter to small fungal VCs. Fungal VCs promoted increases in growth, starch content, and photosynthesis in WT and gpt2-1 plants. These changes were substantially weaker in VC-exposed pgi1-2gpt2-1 plants but reverted to WT levels with vascular and root tip-specific GPT2 expression. Proteomic analyses did not detect enhanced levels of GPT2 protein in VC-exposed leaves and showed that knocking out GPT2 reduced the expression of photosynthesis-related proteins in pgi1-2 plants. Histochemical analyses of GUS activity in plants expressing GPT2-GUS under the control of the GPT2 promoter showed that GPT2 is mainly expressed in root tips and vascular tissues around hydathodes. Overall, the data indicated that the PGI1-independent response to microbial VCs involves resetting of the photosynthesis-related proteome in leaves through long-distance GPT2 action.

Zobrazit více v PubMed

Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56: 1535–1544 PubMed

Alonso C, Ramos-Cruz D, Becker C (2019) The role of plant epigenetics in biotic interactions. New Phytol 221: 731–737 PubMed PMC

Ameztoy K, Baslam M, Sánchez-López ÁM, Muñoz FJ, Bahaji A, Almagro G, García-Gómez P, Baroja-Fernández E, De Diego N, Humplík JF, et al. (2019) Plant responses to fungal volatiles involve global post-translational thiol redox proteome changes that affect photosynthesis. Plant Cell Environ 42: 2627–2644 PubMed

Ameztoy K, Sánchez-López ÁM, Muñoz FJ, Bahaji A, Almagro G, Baroja-Fernández E, Gámez-Arcas S, De Diego N, Doležal K, Novák O, et al. (2021) Proteostatic regulation of MEP and shikimate pathways by redox-activated photosynthesis signaling in plants exposed to small fungal volatiles. Front Plant Sci 12. doi: 10.3389/fpls.2021.637976 PubMed DOI PMC

Arribas-Hernández L, Brodersen P (2020) Occurrence and functions of m6A and other covalent modifications in plant mRNA. Plant Physiol 182: 79–96 PubMed PMC

Athanasiou K, Dyson BC, Webster RE, Johnson GN (2010) Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiol 152: 366–373 PubMed PMC

Backhausen JE, Jöstingmeyer P, Scheibe R (1997) Competitive inhibition of spinach leaf phosphoglucose isomerase isoenzymes by erythrose 4-phosphate. Plant Sci 130: 121–131

Bahaji A, Almagro G, Ezquer I, Gámez-Arcas S, Sánchez-López ÁM, Muñoz FJ, Barrio RJ, Sampedro MC, De Diego N, Spíchal L, et al. (2018) Plastidial phosphoglucose isomerase is an important determinant of seed yield through its involvement in gibberellin-mediated reproductive development and storage reserve biosynthesis in Arabidopsis. Plant Cell 30: 2082–2098 PubMed PMC

Bahaji A, Li J, Ovecka M, Ezquer I, Muñoz FJ, Baroja-Fernández E, Romero JM, Almagro G, Montero M, Hidalgo M, et al. (2011) Arabidopsis thaliana mutants lacking ADP-glucose pyrophosphorylase accumulate starch and wild-type ADP-glucose content: further evidence for the occurrence of important sources, other than ADP-glucose pyrophosphorylase, of ADP-glucose linked to leaf starch biosynthesis. Plant Cell Physiol 52: 1162–1176 PubMed

Bahaji A, Li J, Sánchez-López ÁM, Baroja-Fernández E, Muñoz FJ, Ovecka M, Almagro G, Montero M, Ezquer I, Etxeberria E, et al. (2014) Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol Adv 32: 87–106 PubMed

Bahaji A, Sánchez-López ÁM, De Diego N, Muñoz FJ, Baroja-Fernández E, Li J, Ricarte-Bermejo A, Baslam M, Aranjuelo I, Almagro G, et al. (2015) Plastidic phosphoglucose isomerase is an important determinant of starch accumulation in mesophyll cells, growth, photosynthetic capacity, and biosynthesis of plastidic cytokinins in Arabidopsis. PLoS One 10: e0119641. PubMed PMC

Baroja-Fernández E, Almagro G, Sánchez-López ÁM, Bahaji A, Gámez-Arcas S, De Diego N, Dolezal K, Muñoz FJ, Climent Sanz E, Pozueta-Romero J (2021) Enhanced yield of pepper plants promoted by soil application of volatiles from cell-free fungal culture filtrates is associated with activation of the beneficial soil microbiota. Front Plant Sci 12. doi: 10.3389/fpls.2021.752653 PubMed PMC

Baroja-Fernández E, Muñoz FJ, Li J, Bahaji A, Almagro G, Montero M, Etxeberria E, Hidalgo M, Sesma MT, Pozueta-Romero J (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci USA 109: 321–326 PubMed PMC

Baune M-C, Lansing H, Fischer K, Meyer T, Charton L, Linka N, von Schaewen A (2020) The Arabidopsis plastidial glucose-6-phosphate transporter GPT1 is dually targeted to peroxisomes via the endoplasmic reticulum. Plant Cell 32: 1703–1726 PubMed PMC

Behnam B, Iuchi S, Fujita M, Fujita Y, Takasaki H, Osakabe Y, Yamaguchi-Shinozaki K, Kobayashi M, Shinozaki K (2013) Characterization of the promoter region of an Arabidopsis gene for 9-cis-epoxycarotenoid dioxygenase involved in dehydration-inducible transcription. DNA Res 20: 315–324 PubMed PMC

Berkowitz O, Xu Y, Liew LC, Wang Y, Zhu Y, Hurgobin B, Lewsey MG, Whelan J (2021) RNA-seq analysis of laser microdissected Arabidopsis thaliana leaf epidermis, mesophyll and vasculature defines tissue-specific transcriptional responses to multiple stress treatments. Plant J 107: 938–955 PubMed

Bodi Z, Zhong S, Mehra S, Song J, Graham N, Li H, May S, Fray RG (2012) Adenosine methylation in Arabidopsis mRNA is associated with the 3′ end and reduced levels cause developmental defects. Front Plant Sci 3. doi: 10.3389/fpls.2012.00048 PubMed PMC

Boonman A, Prinsen E, Gilmer F, Schurr U, Peeters AJM, Voesenek LACJ, Pons TL (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiol 143: 1841–1852 PubMed PMC

Bürkle L, Cedzich A, Döpke C, Stransky H, Okumoto S, Gillissen B, Kühn C, Frommer WB (2003) Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J 34: 13–26 PubMed

Camarena-Pozos DA, Flores-Núñez VM, López MG, López-Bucio J, Partida-Martínez LP (2019) Smells from the desert: microbial volatiles that affect plant growth and development of native and non-native plant species. Plant Cell Environ 42: 1368–1380 PubMed

Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burny A, Gras H, Tartar A (1988) The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 332: 454–455 PubMed

Cho MH, Lim H, Shin DH, Jeon JS, Bhoo SH, Park Y Il, Hahn TR (2011) Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. New Phytol 190: 101–112 PubMed

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743 PubMed

Cortleven A, Schmülling T (2015) Regulation of chloroplast development and function by cytokinin. J Exp Bot 66: 4999–5013 PubMed

Cortleven A, Valcke R (2012) Evaluation of the photosynthetic activity in transgenic tobacco plants with altered endogenous cytokinin content: lessons from cytokinin. Physiol Plantarum 144: 394–408 PubMed

Crisp PA, Ganguly DR, Smith AB, Murray KD, Estavillo GM, Searle I, Ford E, Bogdanović O, Lister R, Borevitz JO, et al. (2017) Rapid recovery gene downregulation during excess-light stress and recovery in Arabidopsis. Plant Cell 29: 1836–1863 PubMed PMC

Denison FC, Paul AL, Zupanska AK, Ferl RJ (2011) 14-3-3 proteins in plant physiology. Semin Cell Dev Biol 22: 720–727 PubMed

Dietz KJ (1985) A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis of leaves. BBA - Gen Subj 839: 240–248

Dyson BC, Allwood JW, Feil R, Xu Y, Miller M, Bowsher CG, Goodacre R, Lunn JE, Johnson GN (2015) Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation. Plant Cell Environ 38: 1404–1417 PubMed PMC

Dyson BC, Webster RE, Johnson GN (2014) GPT2: A glucose 6-phosphate/phosphate translocator with a novel role in the regulation of sugar signalling during seedling development. Ann Bot 113: 643–652 PubMed PMC

Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 145: 1–8 PubMed

Flütsch S, Horrer D, Santelia D (2022) Starch biosynthesis in guard cells has features of both autotrophic and heterotrophic tissues. Plant Physiol 189: 541–556 PubMed PMC

Fünfgeld MMFF, Wang W, Ishihara H, Arrivault S, Feil R, Smith AM, Stitt M, Lunn JE, Niittylä T (2022) Sucrose synthases are not involved in starch synthesis in Arabidopsis leaves. Nat Plants 8: 574–582 PubMed PMC

Gámez-Arcas S, Baroja-Fernández E, García-Gómez P, Muñoz FJ, Almagro G, Bahaji A, Sánchez-López ÁM, Pozueta-Romero J (2022) Action mechanisms of small microbial volatile compounds in plants. J Exp Bot 73: 498–510 PubMed

García-Gómez P, Almagro G, Sánchez-López ÁM, Bahaji A, Ameztoy K, Ricarte-Bermejo A, Baslam M, Antolín MC, Urdiain A, López-Belchi MD, et al. (2019) Volatile compounds other than CO2 emitted by different microorganisms promote distinct posttranscriptionally regulated responses in plants. Plant Cell Environ 42: 1729–1746 PubMed

García-Gómez P, Bahaji A, Gámez-Arcas S, Muñoz FJ, Sánchez-lópez ÁM, Almagro G, Baroja-Fernández E, Ameztoy K, De Diego N, Ugena L, et al. (2020) Volatiles from the fungal phytopathogen Penicillium aurantiogriseum modulate root metabolism and architecture through proteome resetting. Plant Cell Environ 43: 2551–2570 PubMed

Garcia-Molina A, Kleine T, Schneider K, Mühlhaus T, Lehmann M, Leister D (2020) Translational components contribute to acclimation responses to high light, heat, and cold in Arabidopsis. iScience 23. doi: 10.1016/j.isci.2020.101331 PubMed PMC

Giese J-O, Herbers K, Hoffmann M, Klösgen RB, Sonnewald U (2005) Isolation and functional characterization of a novel plastidic hexokinase from Nicotiana tabacum. FEBS Lett 579: 827–831 PubMed

Gjindali A, Herrmann HA, Schwartz JM, Johnson GN, Calzadilla PI (2021) A holistic approach to study photosynthetic acclimation responses of plants to fluctuating light. Front Plant Sci 12. doi: 10.3389/fpls.2021.668512 PubMed PMC

Gonzali S, Loreti E, Solfanelli C, Novi G, Alpi A, Perata P (2006) Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis. J Plant Res 119: 115–123 PubMed

Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132: 578–596 PubMed PMC

Hedhly A,, Vogler H,, SchmidMW, , Pazmino D,, Gagliardini V,, Santelia D,, Grossniklaus U (2016) Starch turnover and metabolism during flower and early embryo development. Plant Physiol 172: 2388–2402 PubMed PMC

Hendriks JHM, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133: 838–849 PubMed PMC

Heuer B, Hansen MJ, Anderson LE (1982) Light modulation of phosphofructokinase in pea leaf chloroplasts. Plant Physiol 69: 1404–1406 PubMed PMC

Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184–1194 PubMed

Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH (2017) SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Res 45: D1064–D1074 PubMed PMC

Jefferson R, Kavanagh T, Bevan M (1987) GUS fusion: beta -glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 PubMed PMC

Jeffery C, Bahnson BJ, Chien W, Ringe D, Petsko GA (2000) Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine motility factor, and differentiation mediator. Biochemistry 39: 955–964 PubMed

Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, Flugge UI (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10: 105–117 PubMed PMC

Karim MF (2021) Acclimation of photosynthesis to changes in the environment results in decreases of oxidative stress in Arabidopsis thaliana. Front Plant Sci 12. doi: 10.3389/fpls.2021.683986 PubMed PMC

Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12: e0168. PubMed PMC

Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon MM, Endler A, Song W-YYW-Y, et al. (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci USA 111: 7150–7155 PubMed PMC

Körner C (2015) Paradigm shift in plant growth control. Curr Opin Plant Biol 25: 107–114 PubMed

Kunz HH, Häusler RE, Fettke J, Herbst K, Niewiadomski P, Gierth M, Bell K, Steup M, Flügge UI, Schneider A (2010) The role of plastidial glucose-6-phosphate/phosphate translocators in vegetative tissues of Arabidopsis thaliana mutants impaired in starch biosynthesis. Plant Biol 12: 115–128 PubMed

Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18: 124. PubMed PMC

Lei M, Liu Y, Zhang B, Zhao Y, Wang X, Zhou Y, Raghothama KG, Liu D (2011) Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol 156: 1116–1130 PubMed PMC

Li J, Ezquer I, Bahaji A, Montero M, Ovecka M, Baroja-Fernández E, Muñoz FJ, Mérida Á, Almagro G, Hidalgo M, et al. (2011) Microbial volatile-induced accumulation of exceptionally high levels of starch in Arabidopsis leaves is a process involving NTRC and starch synthase classes III and IV. Mol Plant-Microbe Interact 24: 1165–1178 PubMed

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350–382

Lima JE, Kojima S, Takahashi H, Von Wiren N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22: 3621–3633 PubMed PMC

Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523–536 PubMed PMC

Liu P, Zhang H, Wang H, Xia Y (2014) Identification of redox-sensitive cysteines in the Arabidopsis proteome using OxiTRAQ, a quantitative redox proteomics method. Proteomics 14: 750–762 PubMed

Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54: 2393–2401 PubMed

Makino A, Tadahiko M, Mae T (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol 40: 999–1006

Martínez-Medina A, Van Wees SCM, Pieterse CMJ (2017) Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic aciddependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ 40: 2691–2705 PubMed

McWhite CD, Papoulas O, Drew K, Cox RM, June V, Dong OX, Kwon T, Wan C, Salmi ML, Roux SJ, et al. (2020) A pan-plant protein complex map reveals deep conservation and novel assemblies. Cell 181: 460–474 PubMed PMC

Miller MAE, O’Cualain R, Selley J, Knight D, Karim MF, Hubbard SJ, Johnson GN (2017) Dynamic acclimation to high light in Arabidopsis thaliana involves widespread reengineering of the leaf proteome. Front Plant Sci 8. doi: 10.3389/fpls.2017.01239 PubMed PMC

Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45: 760–775 PubMed

Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128–138 PubMed

Nagawa S, Sawa S, Sato S, Kato T, Tabata S, Fukuda H (2006) Gene trapping in Arabidopsis reveals genes involved in vascular development. Plant Cell Physiol 47: 1394–1405 PubMed

Nakaminami K, Matsui A, Nakagami H, Minami A, Nomura Y, Tanaka M, Morosawa T, Ishida J, Takahashi S, Uemura M, et al. (2014) Analysis of differential expression patterns of mRNA and protein during cold-acclimation and de-acclimation in Arabidopsis. Mol Cell Proteomics 13: 3602–3611 PubMed PMC

Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flügge UI, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17: 760–775 PubMed PMC

Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 2214–2224 PubMed

Pozueta-Romero J, Ardila F, Akazawa T (1991) ADP-Glucose transport by the chloroplast adenylate translocator is linked to starch biosynthesis. Plant Physiol 97: 1565–1572 PubMed PMC

Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150: 889–903 PubMed PMC

Sánchez-López ÁM, Bahaji A, De Diego N, Baslam M, Li J, Muñoz FJ, Almagro G, García-Gómez P, Ameztoy K, Ricarte-Bermejo A, et al. (2016a) Arabidopsis responds to Alternaria alternata volatiles by triggering plastid phosphoglucose isomerase-independent mechanisms. Plant Physiol 172: 1989–2001 PubMed PMC

Sánchez-López ÁM, Baslam M, De Diego N, Muñoz FJ, Bahaji A, Almagro G, Ricarte-Bermejo A, García-Gómez P, Li J, Humplík JF, et al. (2016b) Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ 39: 2592–2608 PubMed

Schwender J, König C, Klapperstück M, Heinzel N, Munz E, Hebbelmann I, Hay JO, Denolf P, De Bodt S, Redestig H, et al. (2014) Transcript abundance on its own cannot be used to infer fluxes in central metabolism. Front Plant Sci 5. doi: 10.3389/fpls.2014.00668 PubMed PMC

Sharifi R, Jeon JS, Ryu CM (2022) Belowground plant-microbe communications via volatile compounds. J Exp Bot 73: 463–486 PubMed

Silverstone AL, Chang CW, Krol E, Sun TP (1997) Developmental regulation of the gibberellin biosynthetic gene GA 1 in Arabidopsis thaliana. Plant J 12: 9–19 PubMed

Steyfkens F, Zhang Z, Van Zeebroeck G, Thevelein JM (2018) Multiple transceptors for macro- and micro-nutrients control diverse cellular properties through the PKA pathway in yeast: a paradigm for the rapidly expanding world of eukaryotic nutrient transceptors up to those in human cells. Front Pharmacol 9. doi: 10.3389/fphar.2018.00191 PubMed PMC

Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914–939 PubMed

van Dingenen J, de Milde L, Vermeersch M, Maleux K, de Rycke R, de Bruyne M, Storme V, Gonzalez N, Dhondt S, Inzé D (2016) Chloroplasts are central players in sugar-induced leaf growth. Plant Physiol 171: 590–605 PubMed PMC

Volpe V, Giovannetti M, Sun XG, Fiorilli V, Bonfante P (2016). The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant Cell Environ 39: 660–671 PubMed

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387 PubMed

Vlot AC, Rosenkranz M (2022) Volatile compounds—the language of all kingdoms? J Exp Bot 73: 445–448 PubMed PMC

Wang X, Bian Y, Cheng K, Gu LF, Ye M, Zou H, Sun SS, He JX (2013) A large-scale protein phosphorylation analysis reveals novel phosphorylation motifs and phosphoregulatory networks in Arabidopsis. J Proteomics 14: 486–498 PubMed

Watanabe H, Takehana K, Date M, Shinozaki T, Raz A (1996) Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 56: 2960–2963 PubMed

Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787–801 PubMed PMC

Weise SE, Liu T, Childs KL, Preiser AL, Katulski HM, Perrin-Porzondek C, Sharkey TD (2019) Transcriptional regulation of the glucose-6-phosphate/phosphate translocator 2 is related to carbon exchange across the chloroplast envelope. Front Plant Sci 10. doi: 10.3389/fpls.2019.00827 PubMed PMC

Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, et al. (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24: 4236–4251 PubMed PMC

Yang T, Sun Y, Wang Y, Zhou L, Chen M, Bian Z, Lian Y, Xuan L, Yuan G, Wang X, et al. (2020) AtHSPR si involved in GA- and light intensity-mediated control of flowering time and seed set in Arabidopsis. J Exp Bot 71: 3543–3559 PubMed PMC

Yin Z, Balmant K, Geng S, Zhu N, Zhang T, Dufresne C, Dai S, Chen S (2017) Bicarbonate induced redox proteome changes in Arabidopsis suspension cells. Front Plant Sci 8. doi: 10.3389/fpls.2017.00058 PubMed PMC

Yu TS, Lue WL, Wang SM, Chen J (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 123: 319–326 PubMed PMC

Žd’árská M, Zatloukalová P, Benítez M, Šedo O, Potěšil D, Novák O, Svačinová J, Pešek B, Malbeck J, Vašíčková J, et al. (2013) Proteome analysis in Arabidopsis reveals shoot- and root-specific targets of cytokinin action and differential regulation of hormonal homeostasis. Plant Physiol 161: 918–930 PubMed PMC

Zhang B, Pasini R, Dan H, Joshi N, Zhao Y, Leustek T, Zheng ZL (2014). Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. Plant J 77: 185–197 PubMed

Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56: 264–273 PubMed

Zhang L, Yang T, Li X, Hao H, Xu S, Cheng W, Sun Y, Wang C (2014) Cloning and characterization of a novel Athspr promoter specifically active in vascular tissue. Plant Physiol Biochem 78: 88–96 PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...