The plastid-localized phosphoglucose isomerase isoform PGI1 is an important determinant of growth in Arabidopsis thaliana, likely due to its involvement in the biosynthesis of plastidial isoprenoid-derived hormones. Here, we investigated whether PGI1 also influences seed yields. PGI1 is strongly expressed in maturing seed embryos and vascular tissues. PGI1-null pgi1-2 plants had ∼60% lower seed yields than wild-type plants, with reduced numbers of inflorescences and thus fewer siliques and seeds per plant. These traits were associated with low bioactive gibberellin (GA) contents. Accordingly, wild-type phenotypes were restored by exogenous GA application. pgi1-2 seeds were lighter and accumulated ∼50% less fatty acids (FAs) and ∼35% less protein than wild-type seeds. Seeds of cytokinin-deficient plants overexpressing CYTOKININ OXIDASE/DEHYDROGENASE1 (35S:AtCKX1) and GA-deficient ga20ox1 ga20ox2 mutants did not accumulate low levels of FAs, and exogenous application of the cytokinin 6-benzylaminopurine and GAs did not rescue the reduced weight and FA content of pgi1-2 seeds. Seeds from reciprocal crosses between pgi1-2 and wild-type plants accumulated wild-type levels of FAs and proteins. Therefore, PGI1 is an important determinant of Arabidopsis seed yield due to its involvement in two processes: GA-mediated reproductive development and the metabolic conversion of plastidial glucose-6-phosphate to storage reserves in the embryo.

Central Service of Analysis of Alava SGIker University of the Basque Country UPV EHU E 01006 Vitoria Gasteiz Spain

Department of Analytical Chemistry Faculty of Pharmacy University of the Basque Country UPV EHU E 01006 Vitoria Gasteiz Spain

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University CZ 78371 Olomouc Czech Republic

Dipartimento di BioScienze Università degli Studi di Milano 20133 Milan Italy

Instituto de Agrobiotecnología 31192 Mutiloabeti Nafarroa Spain

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany AS CR and Faculty of Science Palacký University CZ 78371 Olomouc Czech Republic

Zobrazit více v PubMed

Bahaji A., 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

Barker R. (2011). Gibberellin Biosynthesis and Signalling in Arabidopsis Root Growth. PhD dissertation (Nottingham, UK: University of Nottingham).

Bartrina I., Otto E., Strnad M., Werner T., Schmülling T. (2011). Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23: 69–80. PubMed PMC

Baud S., Wuillème S., Dubreucq B., de Almeida A., Vuagnat C., Lepiniec L., Miquel M., Rochat C. (2007). Function of plastidial pyruvate kinases in seeds of Arabidopsis thaliana. Plant J. 52: 405–419. PubMed

Baud S., Dubreucq B., Miquel M., Rochat C., Lepiniec L. (2008). Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. The Arabidopsis Book 6: e0113, doi/10.1199/tab.0113. PubMed PMC

Bhargava A., Clabaugh I., To J.P., Maxwell B.B., Chiang Y.-H., Schaller G.E., Loraine A., Kieber J.J. (2013). Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 162: 272–294. PubMed PMC

Brenner W.G., Schmülling T. (2015). Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front. Plant Sci. 6: 29. PubMed PMC

Cernac A., Andre C., Hoffmann-Benning S., Benning C. (2006). WRI1 is required for seed germination and seedling establishment. Plant Physiol. 141: 745–757. PubMed PMC

Chen L.-Q., Lin I.W., Qu X.-Q., Sosso D., McFarlane H.E., Londoño A., Samuels A.L., Frommer W.B. (2015). A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27: 607–619. PubMed PMC

Chen M., Du X., Zhu Y., Wang Z., Hua S., Li Z., Guo W., Zhang G., Peng J., Jiang L. (2012a). Seed Fatty Acid Reducer acts downstream of gibberellin signalling pathway to lower seed fatty acid storage in Arabidopsis. Plant Cell Environ. 35: 2155–2169. PubMed

Chen M., Wang Z., Zhu Y., Li Z., Hussain N., Xuan L., Guo W., Zhang G., Jiang L. (2012b). The effect of transparent TESTA2 on seed fatty acid biosynthesis and tolerance to environmental stresses during young seedling establishment in Arabidopsis. Plant Physiol. 160: 1023–1036. PubMed PMC

Chen M., Xuan L., Wang Z., Zhou L., Li Z., Du X., Ali E., Zhang G., Jiang L. (2014). TRANSPARENT TESTA8 inhibits seed fatty acid accumulation by targeting several seed development regulators in Arabidopsis. Plant Physiol. 165: 905–916. PubMed PMC

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

D’Aloia M., Bonhomme D., Bouché F., Tamseddak K., Ormenese S., Torti S., Coupland G., Périlleux C. (2011). Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J. 65: 972–979. PubMed

Eastmond P.J., Rawsthorne S. (1998). Comparison of the metabolic properties of plastids isolated from developing leaves or embryos of Brassica napus L. J. Exp. Bot. 49: 1105–1111.

Eastmond P.J., Rawsthorne S. (2000). Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape embryos. Plant Physiol. 122: 767–774. PubMed PMC

Fleet C.M., Sun T.-P. (2005). A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr. Opin. Plant Biol. 8: 77–85. PubMed

Focks N., Benning C. (1998). wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 118: 91–101. PubMed PMC

Foyer C.H., Noctor G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866–1875. PubMed PMC

Girke T., Todd J., Ruuska S., White J., Benning C., Ohlrogge J. (2000). Microarray analysis of developing Arabidopsis seeds. Plant Physiol. 124: 1570–1581. PubMed PMC

Guo L., Ma F., Wei F., Fanella B., Allen D.K., Wang X. (2014). Cytosolic phosphorylating glyceraldehyde-3-phosphate dehydrogenases affect Arabidopsis cellular metabolism and promote seed oil accumulation. Plant Cell 26: 3023–3035. PubMed PMC

Hayashi M., Toriyama K., Kondo M., Nishimura M. (1998). 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid β-oxidation. Plant Cell 10: 183–195. PubMed PMC

Hedden P., Thomas S.G. (2012). Gibberellin biosynthesis and its regulation. Biochem. J. 444: 11–25. PubMed

Hutchings D., Rawsthorne S., Emes M.J. (2005). Fatty acid synthesis and the oxidative pentose phosphate pathway in developing embryos of oilseed rape (Brassica napus L.). J. Exp. Bot. 56: 577–585. PubMed

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

Jofuku K.D., Omidyar P.K., Gee Z., Okamuro J.K. (2005). Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc. Natl. Acad. Sci. USA 102: 3117–3122. PubMed PMC

Kang F., Rawsthorne S. (1996). Metabolism of glucose-6-phosphate and utilization of multiple metabolites for fatty acid synthesis by plastids from developing oilseed rape embryos. Planta 199: 321–327.

Kiba T., Naitou T., Koizumi N., Yamashino T., Sakakibara H., Mizuno T. (2005). Combinatorial microarray analysis revealing arabidopsis genes implicated in cytokinin responses through the His->Asp Phosphorelay circuitry. Plant Cell Physiol. 46: 339–355. PubMed

Knappe S., Löttgert T., Schneider A., Voll L., Flügge U.-I., Fischer K. (2003). Characterization of two functional phosphoenolpyruvate/phosphate translocator (PPT) genes in Arabidopsis--AtPPT1 may be involved in the provision of signals for correct mesophyll development. Plant J. 36: 411–420. PubMed

Lee D.J., Zeevaart J.A.D. (2007). Regulation of gibberellin 20-oxidase1 expression in spinach by photoperiod. Planta 226: 35–44. PubMed

Lee E.-J., Oh M., Hwang J.-U., Li-Beisson Y., Nishida I., Lee Y. (2017). Seed-specific overexpression of the pyruvate transporter BASS2 increases oil content in Arabidopsis seeds. Front. Plant Sci. 8: 194. 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

Lonien J., Schwender J. (2009). Analysis of metabolic flux phenotypes for two Arabidopsis mutants with severe impairment in seed storage lipid synthesis. Plant Physiol. 151: 1617–1634. PubMed PMC

Magome H., Yamaguchi S., Hanada A., Kamiya Y., Oda K. (2004). dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J. 37: 720–729. PubMed

Meng L., Feldman L. (2010). A rapid TRIzol-based two-step method for DNA-free RNA extraction from Arabidopsis siliques and dry seeds. Biotechnol. J. 5: 183–186. PubMed

Mitchum M.G., Yamaguchi S., Hanada A., Kuwahara A., Yoshioka Y., Kato T., Tabata S., Kamiya Y., Sun T.P. (2006). Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J. 45: 804–818. 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

Mustroph A., Sonnewald U., Biemelt S. (2007). Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana. FEBS Lett. 581: 2401–2410. PubMed

Mutasa-Göttgens E., Hedden P. (2009). Gibberellin as a factor in floral regulatory networks. J. Exp. Bot. 60: 1979–1989. PubMed

Née G., Zaffagnini M., Trost P., Issakidis-Bourguet E. (2009). Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett. 583: 2827–2832. PubMed

Pokhilko A., Bou-Torrent J., Pulido P., Rodríguez-Concepción M., Ebenhöh O. (2015). Mathematical modelling of the diurnal regulation of the MEP pathway in Arabidopsis. New Phytol. 206: 1075–1085. PubMed

Prabhakar V., et al. (2010). Phosphoenolpyruvate provision to plastids is essential for gametophyte and sporophyte development in Arabidopsis thaliana. Plant Cell 22: 2594–2617. PubMed PMC

Pulido P., Perello C., Rodríguez-Concepción M. (2012). New insights into plant isoprenoid metabolism. Mol. Plant 5: 964–967. PubMed

Reiser J., Linka N., Lemke L., Jeblick W., Neuhaus H.E. (2004). Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis. Plant Physiol. 136: 3524–3536. PubMed PMC

Riefler M., Novak O., Strnad M., Schmülling T. (2006). Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40–54. PubMed PMC

Rieu I., Eriksson S., Powers S.J., Gong F., Griffiths J., Woolley L., Benlloch R., Nilsson O., Thomas S.G., Hedden P., Phillips A.L. (2008a). Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20: 2420–2436. PubMed PMC

Rieu I., Ruiz-Rivero O., Fernández-García N., Griffiths J., Powers S.J., Gong F., Linhartova T., Eriksson S., Nilsson O., Thomas S.G., Phillips A.L., Hedden P. (2008b). The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J. 53: 488–504. PubMed

Rittenberg D., Foster G.L. (1940). A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133: 737–744.

Ruuska S.A., Girke T., Benning C., Ohlrogge J.B. (2002). Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14: 1191–1206. PubMed PMC

Sánchez-López Á.M., et al. (2016). Arabidopsis responds to Alternaria alternata volatiles by triggering plastid phosphoglucose isomerase-independent mechanisms. Plant Physiol. 172: 1989–2001. PubMed PMC

Schwender J., Ohlrogge J.B., Shachar-Hill Y. (2003). A flux model of glycolysis and the oxidative pentosephosphate pathway in developing Brassica napus embryos. J. Biol. Chem. 278: 29442–29453. PubMed

Schwender J., Goffman F., Ohlrogge J.B., Shachar-Hill Y. (2004). Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432: 779–782. PubMed

Silverstone A.L., Chang C., Krol E., Sun T.P. (1997). Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 12: 9–19. PubMed

Spíchal L. (2012). Cytokinins-recent news and views of evolutionally old molecules. Funct. Plant Biol. 39: 267–284. PubMed

Tsai H.L., Lue W.L., Lu K.J., Hsieh M.H., Wang S.M., Chen J. (2009). Starch synthesis in Arabidopsis is achieved by spatial cotranscription of core starch metabolism genes. Plant Physiol. 151: 1582–1595. PubMed PMC

Urbanová T., Tarkowská D., Novák O., Hedden P., Strnad M. (2013). Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112: 85–94. PubMed

Van Daele I., Gonzalez N., Vercauteren I., de Smet L., Inzé D., Roldán-Ruiz I., Vuylsteke M. (2012). A comparative study of seed yield parameters in Arabidopsis thaliana mutants and transgenics. Plant Biotechnol. J. 10: 488–500. PubMed

Ventriglia T., Kuhn M.L., Ruiz M.T., Ribeiro-Pedro M., Valverde F., Ballicora M.A., Preiss J., Romero J.M. (2008). Two Arabidopsis ADP-glucose pyrophosphorylase large subunits (APL1 and APL2) are catalytic. Plant Physiol. 148: 65–76. PubMed PMC

Voinnet O., Pinto Y.M., Baulcombe D.C. (1999). Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96: 14147–14152. PubMed PMC

Werner T., Motyka V., Laucou V., Smets R., Van Onckelen H., Schmülling T. (2003). Cytokinin-deficient transgenic Arabidopsis plants show functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532–2550. PubMed PMC

White J.A., Todd J., Newman T., Focks N., Girke T., de Ilárduya O.M., Jaworski J.G., Ohlrogge J.B., Benning C. (2000). A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. Plant Physiol. 124: 1582–1594. PubMed PMC

Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. (2007). An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718. PubMed PMC

Yamaguchi S. (2008). Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59: 225–251. PubMed

Yamaguchi N., Winter C.M., Wu M.-F., Kanno Y., Yamaguchi A., Seo M., Wagner D. (2014). Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344: 638–641. PubMed

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: 58. PubMed PMC

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

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