[en] Previous studies on Arabidopsis under long-term exposure to elevated CO2 have been conducted using starch synthesis and breakdown mutants cultured under short day conditions. These studies showed that starch synthesis can ameliorate the photosynthetic reduction caused by soluble sugar-mediated feedback regulation. In this work we characterized the effect of long-term exposure to elevated CO2 (800 ppm) on growth, photosynthesis and content of primary photosynthates in long-day grown wild type plants as well as the near starch-less (aps1) and the starch-excess (gwd) mutants. Notably, elevated CO2 promoted growth of both wild type and aps1 plants but had no effect on gwd plants. Growth promotion by elevated CO2 was accompanied by an increased net photosynthesis in WT and aps1 plants. However, the plants with the highest starch content (wild type at elevated CO2, gwd at ambient CO2, and gwd at elevated CO2) were the ones that suffered decreased in in vivo maximum carboxylation rate of Rubisco, and therefore, photosynthetic down-regulation. Further, the photosynthetic rates of wild type at elevated CO2 and gwd at elevated CO2 were acclimated to elevated CO2. Notably, elevated CO2 promoted the accumulation of stress-responsive and senescence-associated amino acid markers in gwd plants. The results presented in this work provide evidence that under long-day conditions, temporary storage of overflow photosynthate as starch negatively affect Rubisco performance. These data are consistent with earlier hypothesis that photosynthetic acclimation can be caused by accelerated senescence and hindrance of CO2 diffusion to the stroma due to accumulation of large starch granules.
Jauregui, Ivan ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions végétales et valorisation
Pozueta-Romero, Javier
Córdoba Jacoste, Francisco Javier ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Avice, Jean-Christophe
Aparicio-Tejo, Pedro M
Baroja-Fernandez, Edurne
Aranjuelo, Iker
Language :
English
Title :
Unraveling the role of transient starch in the response of Arabidopsis to elevated CO 2 under long-day conditions
Ainsworth, E.A., Rogers, A., The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ. 30 (2007), 258–270.
Ainsworth, E.A., Rogers, A., Nelson, R., Long, S.P., Testing the “source–sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agric. For. Meteorol. 122 (2004), 85–94.
Aranjuelo, I., Cabrera-Bosquet, L., Morcuende, R., Avice, J., Nogués, S., Araus, J., Martínez-Carrasco, R., Pérez, P., Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2?. J. Exp. Bot. 62 (2011), 3957–3969.
Aranjuelo, I., Sanz-Sáez, Á., Jauregui, I., Irigoyen, J.J., Araus, J.L., Sánchez-Díaz, M., Erice, G., Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2. J. Exp. Bot. 64 (2013), 1879–1892.
Avila-Ospina, L., Marmagne, A., Talbotec, J., Krupinska, K., Masclaux-Daubresse, C., The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L.), and their expression during leaf senescence. J. Exp. Bot. 66 (2015), 2013–2026.
Bahaji, A., Li, J., Sánchez-López, Á.M., Baroja-Fernández, E., Muñoz, F.J., Ovecka, M., Almagro, G., Montero, M., Ezquer, I., Etxeberria, E., Pozueta-Romero, J., Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol. Adv. 32 (2014), 87–106.
Bahaji, A., Sánchez-López, A.M., De Diego, N., Muñoz, F.J., Baroja-Fernández, E., Li, J., Ricarte-Bermejo, A., Baslam, M., Aranjuelo, I., Almagro, G., Humpilk, J.F., Novák, O., Spichal, L., Dolezal, K., Pozueta-Romero, J., 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, 2015, 10.1371/journal.pone.0119641.
Baslam, M., Baroja-Fernández, E., Sánchez-López, A.M., Aranjuelo, I., Ricarte-Bermejo, A., Bahaji, A., Muñoz, F.J., Almagro, G., Pujol, P., Galarza, R., Teixidor, P., Pozueta-Romero, J., Isotope ratio mass spectrometric and genetic evidence for the occurrence of starch degradation and cycling in illuminated Arabidopsis leaves. PLOS One, 2017, 10.1371/journal.pone.0171245.
Bloom, A.J., Burger, M., Rubio Asensio, J.S., Cousins, A.B., Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328 (2010), 899–903.
Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R., Görlach, J., Growth stage-based phenotypic analysis of Arabidopsis: a mmodel for high throughput functional genomics in plants. Plant Cell 13 (2001), 1499–1510.
Caspar, T., Huber, S.C., Somerville, C.R., Alterations in growth, photosynthesis and respiration in a starch deficient mutant of Arabidopsis thaliana (L.) Heynh deficient in chloroplast phosphoglucomutase. Plant Physiol. 79 (1985), 11–17.
Caspar, T., Lin, T.P., Kakefuda, G., Benbow, L., Preiss, J., Somerville, C., Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol. 95 (1991), 1181–1188.
Cheng, S.-H., Moore, B., Seemann, J.R., Effects of short- and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiol. 116 (1998), 715–723.
Cho, M.H., Lim, H., Shin, D.H., Jeon, J.S., Bhoo, S.H., Park, Y.I., Hahn, T.R., Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplast in Arabidopsis thaliana. New Phytol. 190 (2011), 101–112.
Gibon, Y., Bläsing, O.E., Palacios-Rojas, N., Pankovic, D., Hendriks, J.H.M., Fisahn, J., Höhne, M., Günther, M., Stitt, M., Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J. 39 (2004), 847–862.
Gibson, K., Park, J.-S., Nagai, Y., Hwang, S.-K., Cho, Y.-C., Roh, K.-H., Lee, S.-M., Kim, D.-H., Choi, S.-B., Ito, H., Edwards, G.E., Okita, T.W., Exploiting leaf starch synthesis as a transient sink to elevate photosynthesis, plant productivity and yields. Plant Sci. 181 (2011), 275–281.
Huffaker, R.C., Proteolytic activity during senescence of plants. New. Phytol. 116 (1990), 199–231.
IPCC, Summary for policymakers. Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M., (eds.) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 2013, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA.
Jauregui, I., Aparicio-Tejo, P.M., Avila, C., Sakalauskienė S., Aranjuelo, I., Root-shoot interactions explain the reduction of leaf mineral content in Arabidopsis plants grown under elevated [CO2] conditions. Physiol. Plant 158 (2016), 65–79.
Jauregui, I., Aparicio-Tejo, P.M., Baroja, E., Avila, C., Aranjuelo, I., Elevated CO2 improved the growth of a double nitrate reductase defective mutant of Arabidopsis thaliana: The importance of maintaining a high energy status. Environ. Exp. Bot. 140 (2017), 110–119.
Kitao, M., Yazaki, K., Kitaoka, S., Fukatsu, E., Tobita, H., Komatsu, M., Maruyama, Y., Koike, T., Mesophyll conductance in leaves of Japanese white birch (Betula platyphylla var. japonica) seedlings grown under elevated CO2 concentration and low N availability. Physiol. Plant 155 (2015), 435–445.
Lea, P.J., Sodek, L., Parry, M.A.J., Shewry, P.R., Halford, N.G., Asparagine in plants. Ann. Appl. Biol. 150 (2007), 1–26.
Leakey, A.D.B., Ainsworth, E.A., Bernacchi, C.J., Rogers, A., Long, S.P., Ort, D.R., Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60 (2009), 2859–2876.
Li, J., Almagro, G., Muñoz, F.J., Baroja-Fernández, E., Bahaji, A., Montero, M., Hidalgo, M., Sánchez, M.A., Ezquer, I., Sesma, M.T., Pozueta-Romero, J., Posttranslational redox modification of ADP-glucose pyrophosphorylase in response to light is not a major determinant of fine regulation of transitory starch accumulation in Arabidopsis leaves. Plant Cell Physiol. 53 (2012), 433–444.
Long, S.P., Ainsworth, E.A., Rogers, A., Ort, D.R., Rising atmospheric carbon dioxide: plants FACE the future. Annu. Rev. Plant Biol. 55 (2004), 591–628.
Ludewig, F., Sonnewald, U., High CO2-mediated down-regulation of photosynthetic gene transcripts is caused by accelerated leaf senescence rather than sugar accumulation. FEBS Lett. 479 (2000), 19–24.
Makino, A., Mae, T., Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol. 40 (1999), 999–1006.
Markelz, R.J.C., Lai, L.X., Vosseler, L.N., Leakey, A.D.B., Transcriptional reprogramming and stimulation of leaf respiration by elevated CO2 concentration is diminished, but not eliminated, under limiting nitrogen supply. Plant Cell Environ. 37 (2013), 886–898.
Masclaux-Daubresse, C., Reisdorf-Cren, M., Orsel, M., Leaf nitrogen remobilisation for plant development and grain filling. Plant Biol. 10 (2008), 23–36.
McMurtrie, R.E., Wang, Y.-P., Mathematical models of the photosynthetic responses of tree stands to rising CO2 concentrations and temperatures. Plant Cell Environ. 16 (1993), 1–13.
Miller, A., Tsai, C.-H., Hemphill, D., Endres, M., Rodermel, S., Spalding, M., Elevated CO2 effects during leaf ontogeny. Plant Physiol. 115 (1997), 1195–1200.
Moore, B.D., Cheng, S., Sims, D., Seemann, J., The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ. 22 (1999), 567–582.
Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.-H., Liu, Y.-X., Hwang, I., Jones, T., Sheen, J., Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300 (2003), 332–336.
Nafziger, E.D., Koller, R., Influence of leaf starch concentration on CO2 assimilation in soybean. Plant Physiol. 57 (1976), 560–563.
Nakano, H., Muramatsu, S., Makino, A., Mae, T., Relationship between the suppression of photosynthesis and starch accumulation in the pod-removed bean. Aust. J. Plant. Physiol. 27 (2000), 167–173.
Pritchard, S.G., Peterson, C.M., Prior, S.A., Rogers, H.H., Elevated atmospheric CO2 differentially affects needle chloroplast ultrastructure and phloem anatomy in Pinus palustris: interactions with soil resoruce availability. Plant Cell Environ. 20 (1997), 461–471.
Ragel, P., Streb, S., Feil, R., Sahrawy, M., Annunziata, M.G., Lunn, J.E., Zeeman, S., Mérida, Á., Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol. 163 (2013), 75–85.
Rao, M., Terry, N., Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. Plant Physiol. 107 (1995), 195–202.
Rasse, D.P., Tocquin, P., Leaf carbohydrate controls over Arabidopsis growth and response to elevated CO2: an experimentally based model. New Phytol. 172 (2006), 500–513.
Rocha, M., Licausi, F., Araújo, W.L., Nunes-Nesi, A., Sodek, L., Fernie, A.R., van Dongen, J.T., Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced in waterlogging of Lotus japonicus. Plant. Physiol. 152 (2010), 1501–1513.
Sage, R.F., Sharkey, T.D., Seemann, J.R., Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol. 89 (1989), 590–596.
Sánchez-López, A.M., Bahaji, A., De Diego, N., Baslam, M., Li, J., Muñoz, F.J., Almagro, G., García-Gómez, P., Ameztoy, K., Ricarte-Bermejo, A., Novák, O., Humplík, J.F., Spíchal, L., Doležal, K., Ciordia, S., Mena, M.C., Baroja-Fernández, E., Pozueta-Romero, J., Arabidopsis responds to Alternaria alternata volatiles by triggering pPGI-independent mechanisms. Plant Physiol. 172 (2016), 1989–2001.
Santelia, D., Trost, P., Sparla, F., New insights into redox control of starch degradation. Curr. Opin. Plant Biol. 25 (2015), 1–9.
Sawada, S., Kuninaka, M., Watanabe, K., Sato, A., Kawamura, H., Komine, K., Sakamoto, T., Kasai, M., The mechanism to suppress photosynthesis through end-product inhibition in single-rooted soybean leaves during acclimation to CO2 enrichment. Plant Cell Physiol. 42 (2001), 1093–1102.
Singsaas, E.L., Ort, D.R., Delucia, E.H., Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology. Plant Cell Environ. 27 (2004), 41–50.
Stitt, M., Krapp, A., The interaction between elevated carbon dioxide and nitrogen nutrition : the physiological and molecular background. Plant Cell Environ. 22 (1999), 583–621.
Sun, J., Okita, T.W., Edwards, G.E., Modification of carbon partitioning, photosynthetic capacity, and O2 sensitivity in Arabidopsis plants with low ADP-glucose pyrophosphorylase activity. Plant Physiol. 119 (1999), 267–276.
Sun, J., Gibson, K.M., Kiirats, O., Okita, T.W., Edwards, G.E., Interactions of nitrate and CO2 enrichment on growth, carbohydrates, and rubisco in Arabidopsis starch mutants. Significance of starch and hexose. Plant Physiol. 130 (2002), 1573–1583.
Ventriglia, T., Kuhn, M.L., Ruiz, M.T., Ribeiro-Pedro, M., Valverde, F., Ballicora, Preiss, J., Romero, J.M., Two Arabidopsis ADP-glucose pyrophosphorylase large subunits (APL1 and APL2) are catalytic. Plant Physiol. 148 (2008), 65–76.
Wallace, W., Secor, J., Schrader, L.E., Rapid accumulation of γ-aminobutyric acid and alanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or mechanical manipulation. Plant Physiol. 75 (1984), 170–175.
Watanabe, M., Balazadeh, S., Tohge, T., Erban, A., Giavalisco, P., Kopka, J., Mueller-Roeber, B., Fernie, A.R., Hoefgen, R., Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol. 162 (2013), 1290–1310.
Yelle, S., Beeson, R.C., Trudel, M.J., Gosselin, A., Acclimation of two tomato species to high atmospheric CO2. Plant Physiol. 90 (1989), 1465–1472.
