Plant Responses to CO2: Background and Perspectives Ichiro Terashima1,*, Shuichi Yanagisawa2 and Hitoshi Sakakibara3 1
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan 3 Riken Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan *Corresponding author: E-mail, [email protected]; Fax: +81-3-5841-4465 2
Background
Downloaded from http://pcp.oxfordjournals.org/ at Mount Allison University on June 29, 2015
For the past 800,000 years, the atmospheric CO2 concentration, [CO2], has fluctuated between 180–200 and 250–280 ppmv during the different glacial and interglacial periods, respectively (Lu¨thi et al. 2008). Currently, we are in an interglacial period, where [CO2] had been around 280 ppmv for more than 10,000 years and up until the industrial revolution of the 1800s. Since then, [CO2] has been increasing with annual fluctuations peaking in winter, and the most recent peaks exceeding 400 ppmv. The increasing concentration rate has accelerated to the extent that atmospheric CO2 levels may reach twice those before the industrial revolution by the end of this century. This marked increase in [CO2] is the most influential cause of global warming (IPCC, 2013). Higher temperatures and increased [CO2] both pose serious problems to the environment and in particular to plants. This is because plants cannot keep pace with this rapid increase in [CO2] by means of adaptation alone, as most plants are adapted to an atmospheric [CO2] of below 300 ppmv. In 1957, Keeling and his group initiated continuous measurements of atmospheric [CO2] at the summit of Mauna Loa (e.g. Keeling et al. 1996), which continue to show an impressive increasing pattern of [CO2]. Stimulated by the importance of this issue, CO2 doubling growth experiments followed in the 1970s’. Arp (1991) meta-analysed the results of CO2 doubling experiments conducted up to 1990 and showed that enhancement of photosynthetic rates by high [CO2] was only observed in plants grown in very large pots or in fields. In experiments where plants were grown in small pots, photosynthesis was notably downregulated under high [CO2]; this phenomenon became known as the ‘pot size effect.’ From the mid 1990’s, large-scale experiments using open-top chambers or free air CO2 enrichment (FACE) systems were established to circumvent the pot size effect. The results of these large-scale experiments, however, still showed large variations even within the same species (e.g. Hasegawa et al. 2013) and clearly demonstrated that high [CO2] does not necessarily enhance plant growth or crop yield (Makino and Mae 1999, Ainsworth and Long 2005, Luo et al. 2006, Leakey et al. 2009). Thus the precise
effects of CO2 on plant growth and performance remain largely unknown. Because [CO2] will continue to rise for at least another several decades even according to the most optimistic predictions by the IPCC (2013), and because many plant functions are downregulated by high [CO2], it is vital that the detrimental effects of high [CO2] on plants are understood, and ways to overcome these effects sought. Since 2011, we have been running a five-year research project entitled ‘Comprehensive studies of plant responses to the high CO2 world by an innovative consortium of ecologists and molecular biologists’ supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT). In this special focus issue, some representative outputs from this consortium project have been compiled.
Stomata and mesophyll conductance It is widely known that in many angiosperm species the stomata close in response to high [CO2]. Several Arabidopsis thaliana mutants showing impaired stomatal responses to CO2 have been isolated using a high-throughput technique employing thermography of rosette leaves, and analysed (Hashimoto et al. 2006, Negi et al. 2008, Negi et al. 2013, HashimotoSugimoto et al. 2013). Negi et al. (2014) review these seminal studies. In addition, mobile water soluble signal(s) derived from the mesophyll of Commelina communis plants were shown to greatly accelerate guard cell responses to CO2 (Fujita et al. 2013), however, their identity remain unknown. Aquaporins have been implicated in regulating stomatal behaviour, mesophyll conductance for CO2 diffusion (Terashima et al. 2006), and leaf hydraulic conductance (Lopez et al. 2013). Although most studies so far have claimed that plasma membrane intrinsic protein 2 (PIP2)-type aquaporins are water channels, on pp. 251–257 Mori et al. (2014) clearly demonstrate that some barley (Hordeum vulgare) HvPIP2 aquaporins, including HvPIP2;1, act as CO2 channels, and identified the amino acid residue that is responsible for CO2 permeability. In addition, it was shown previously that overexpression of HvPIP2;1 in rice (Oryza sativa) increased mesophyll conductance for CO2 diffusion (Hanba et al. 2004). Thus, it would appear that some
Plant Cell Physiol. 55(2): 237–240 (2014) doi:10.1093/pcp/pcu022, available online at www.pcp.oxfordjournals.org ! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 55(2): 237–240 (2014) doi:10.1093/pcp/pcu022 ! The Author 2014.
237
aquaporins actually facilitate CO2 transfer and increase mesophyll conductance. In such cases, these aquaporins would be more appropriately called cooporins as previously proposed by Terashima et al. (2006). The next step would be to determine specific regulation mechanisms of leaf aquaporins and cooporins in a comprehensive manner.
C/N balance, Sato et al. (2009, 2011) identified the ubiquitin ligase CNI1/ATL31 as a novel C/N regulator. In these studies, C levels were manipulated with glucose or sucrose in the rooting medium. More recently, Aoyama et al. (2014), however, treated A. thaliana plants with high [CO2] instead of sugar and found that ATL31 is involved in promoting leaf senescence at high [CO2] and low N nutrition.
Plant development
C/N balance and the sink-source relationship At high [CO2] plants tend to accumulate sugar and decrease their nitrogen content, leading to a high C/N ratio in the plant body. Takatani et al. (2014), devised a unique experimental system with an A. thaliana mutant showing reduced nitrate uptake activity to study the nature of the C/N balance. At high [CO2] the mutant suffered from N stress when grown with nitrate, and exhibited some phenotypic features similar to those of wild-type plants subjected to N stress, such as a reduced shoot/root ratio, whereas metabolite levels remained unchanged even under high [CO2]. Thus this experimental system is an effective tool to help uncover plant response mechanisms to high [CO2]. In other work focusing on the
238
Metabolism, respiration and translocation On pp. 306–319, Sato and Yanagisawa (2014) compares metabolite contents in A. thaliana grown with various concentrations of nitrate and/or ammonium and at various [CO2] and light levels. When N and light were sufficient, plant growth was enhanced with [CO2] up to 3600 ppmv, indicating A. thaliana’s potential to utilize CO2 at very high concentrations. It was also revealed that ammonium exerted drastic effects on metabolite patterns regardless of [CO2] levels. In a separate study using rice, Kaneko et al. assessed knockout mutants of nucleotide pyrophosphatase/ phosphodiesterase 1 (npp1) grown at high [CO2] and high temperatures. The results indicate that NPP1, a unique glycoprotein (Nanjo et al. 2006, Kaneko et al. 2011), exerts negative effects on growth and starch accumulation in plants grown at high [CO2] and high temperatures. Manipulation of NPP1 expression levels could potentially be a way to improve rice growth in the high CO2 era. On pp. 333–340, Takagi et al. (2014) show that methylglyoxal, a sugar-derived reactive carbonyl, was produced as a by-product of the triosephosphate isomerase reaction in the Calvin-Benson cycle in wheat (Triticum aestivum) chloroplasts and intact leaves. The production rate of methylglyoxal was dependent on light intensity and [CO2] and could lead to serious oxidative stress, called ‘plant diabetes’ (Saito et al. 2011). In the high CO2 era, it will be necessary to enhance protection mechanisms against this type of stress. Distinction of respiratory characteristics of A. thaliana shoots grown at 390 ppmv and those grown at 780 ppmv CO2 was the focus of a study by Watanabe et al. (2014). Respiration was limited by either substrate supply or demand for ATP in ATP-utilising reactions. At high [CO2], especially towards the end of the dark period, the rate of respiratory O2 uptake was limited by the demand for ATP, suggesting that respiration at high [CO2] tends to be limited by some anabolic processes. In this context, the alternative respiratory pathway may contribute to balancing the NAD(P)H/ATP ratio (Gandin et al. 2013). Duan et al. (2014) examined the impact of high [CO2] on sugar translocation systems in A. thaliana plants, such as abundance of plasmodesmata, and gene expression levels of the sucrose effluxer SWEET12 and sucrose transporters SUC2 and SUT4. They also examined the rates of assimilation and translocation using a 14CO2 tracer. The sugar translocation system changed considerably in response to high [CO2], with differences being observed between the first and third rosette leaves.
Plant Cell Physiol. 55(2): 237–240 (2014) doi:10.1093/pcp/pcu022 ! The Author 2014.
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Plant structural traits such as the shoot to root ratio, leaf thickness, and stomatal density can be modified at high [CO2]. Taking advantage of precise developmental studies of rice leaves (e.g. Yamazaki 1963), Tsutsumi et al. (2014) conducted a detailed developmental study employing transfer experiments, in which plants containing leaves at various developmental stages were transferred from ambient to high CO2 conditions. They succeeded in pinpointing the stages most sensitive to high [CO2] for various leaf morphological traits including leaf length, width, and blade thickness. Stomatal density and index, often reported to decrease at high [CO2] (e.g. Lake et al. 2001), were unchanged, however. These exciting results will form an invaluable basis for the future identification of factors responsible for these morphological and anatomical changes in response to high [CO2]. It is feasible that the shoot to root ratio may respond to changing [CO2], although some meta-analysis studies have not detected such tendencies (Poorter and Nagel, 2000). On pp. 269–280, Hachiya et al. (2014) analysed combined effects of low-medium pH and high CO2, or low nitrogen (N) stress and high [CO2] on growth of A. thaliana. The results clearly indicate that both of these combined conditions caused preferential root growth, but via different mechanisms. In low pH stress and high [CO2], accumulation of sugar caused a change in the auxin and cytokinin balance in a way that favors lateral root growth. Future experiments conducted under several growth conditions and with different relevant mutants (e.g. Hachiya et al. 2012) will be indispensable to further clarify mechanisms of changes in the shoot to root ratio in response to high [CO2].
These results highlight the plastic nature of the translocation system.
Rice FACE
Future scope Within this century, we will soon face a high CO2 era. It is highly likely that the majority of plants, which are adapted to an atmospheric [CO2] of below 300 ppmv, will suffer various detrimental effects. Thus, it is vital to continue research into this field, namely through large-scale growth experiments as well as precise molecular physiological studies, to clarify the respective mechanisms responsible for the various downregulations that occur under high CO2 conditions. Information gleaned from such studies could be used to optimize plant performance under various environmental conditions in a tailor-made manner, and generate valuable materials for breeding. To this aim, effective collaboration between ecologists, agronomists and molecular biologists is indispensable. Without these concerted efforts, we will not be able to increase biomass production, feed the 10 billion people estimated to populate the planet (Evans 1998), or maintain ecosystems that efficiently fix CO2 in the high CO2 era.
Funding This work and the studies compiled in this special issue were supported by a Grant-in-Aid for Scientific Research on Innovative Areas for “Comprehensive studies of plant responses to the high CO2 world by an innovative consortium of ecologists and molecular biologists.”
We thank professor Tomoyuki Yamaya, Editor-in-Chief of Plant and Cell Physiology, for providing us with the opportunity to showcase some of our work in this Special Focus Issue on Plant Response to CO2.
References Adachi, M., Hasegawa, T., Fukayama, H., Tokida, T., Sakai, H., Matsunami, T. et al. (2014) Soil and water warming accelerates phenology and down-regulation of leaf photosynthesis of rice plants grown under free-air CO2 enrichment (FACE). Plant Cell Physiol. 55: 370–380. Ainsworth, E.A. and Long, S.T. (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 165: 351–372. Aoyama, S., Reyes, T.H., Guglielminetti, L., Lu, Y., Morita, Y., Sato, T. et al. (2014) Ubiquitin ligase ATL31 functions in leaf senescence in response to the balance between atmospheric CO2 and nitrogen availability in Arabidopsis. Plant Cell Physiol. 55: 293–305. Arp, W.J. (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Env. 14: 869–875. Chen, C.P., Sakai, H., Tokida, T., Usui, Y., Nakamura, H. and Hasegawa, T. (2014) Do the rich always become richer? Characterizing the leaf physiological response of the highyielding rice cultivar Takanari to free-air CO2 enrichment. Plant Cell Physiol. 55: 381–391. Duan, Z., Homma, A., Kobayashi, M., Nagata, N., Kaneko, Y., Fujiki, Y. et al. (2014) Photoassimilation, assimilate translocation and plasmodesmal biogenesis in the source leaves of Arabidopsis thaliana grown under an increased atmospheric CO2 concentration. Plant Cell Physiol. 55: 358–369. Evans, L.T. (1998) Feeding the Ten Billion. Cambridge Univ. Press, Cambridge. Fujita, T., Noguchi, K. and Terashima, I. (2013) Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol. 199: 395–406. Gandin, A., Duffes, C., Day, D.A. and Cousins, A.B. (2012) The absence of alternative oxidase AOX1A results in altered response of photosynthetic carbon assimilation to increasing CO2 in Arabidopsis thaliana. Plant Cell Physiol. 53: 1627–1637. Hachiya, T., Sugiura, D., Kojima, M., Sato, S., Yanagisawa, S., Sakakibara, H. et al. (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol. 55: 269–280. Hachiya, T., Watanabe, C.K., Fujimoto, M., Ishikawa, T., Takahara, K., Kawai-Yamada, M. et al. (2012) Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots. Plant Cell Physiol. 53: 577–591. Hanba, Y.T., Shibasaka, M., Hayashi, Y., Hayakawa, T., Sasamo, K., Terashima, I. et al. (2004) Overexpression of the barley aquaporin HvPIP1;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol. 45: 521–529. Hasegawa, T., Sakai, H., Tokida, T., Nakamura, H., Zhu, C., Usui, Y. et al. (2013) Rice cultivar response to elevated CO2 at two free-air CO2 enrichment (FACE) sites in Japan. Funct. Plant Biol. 40: 148–159.
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In 1998, a team led by Kobayashi and Okada initiated the FACE project for paddy field rice (Kobayashi et al. 2006), and the lowcost light-weighted FACE facility operating in a pure CO2 injection mode developed by this team (Okada et al. 2001) has now been adopted in most FACE experiments using herbaceous plants. This team has been systematically producing data (e.g. Hasegawa et al. 2013) that will form a fundamental basis for sustainable rice production in the high CO2 era. Adachi et al. (2014) report the combined effects of high [CO2] and an increase in soil and water temperature by 2 C on rice production. High soil and water temperatures under high [CO2] accelerated downregulation or aging of the leaf photosynthetic capacity. In a different study, Chen et al. (2014) compared leaf photosynthetic properties between ambient and elevated [CO2] levels in a high-yielding indica variety (Takanari) and a popular japonica variety (Koshihikari). Takanari showed greater leaf photosynthesis and stomatal conductance as well as increased mesophyll conductance at both [CO2] levels. It is worth noting that leaf N on an area basis was not suppressed by high [CO2] in Takanari. These results indicate that Takanari will be an invaluable resource for rice breeding in the high CO2 era.
Acknowledgement
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Negi, J., Matuda, O., Nagasawa, T., Oba, Y., Takahashi, H., KawaiYamada, M. et al. (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452: 483–486. Negi, J., Morikawa, K., Konishi, M., Yokoyama, R., Nakano, T., Kusumi, K. et al. (2013) A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr. Biol. 23: 479–486. Okada, M., Lieffering, M., Nakamura, H., Yoshimoto, M., Kim, H.Y. and Kobayashi, K. (2001) Free-air CO2 enrichment (FACE) using pure CO2 injection: system description. New Phytol. 150: 251–260. Poorter, H. and Nagel, O. (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust. J. Plant Physiol. 27: 595–607. Saito, R., Yamamoto, H., Makino, A., Sugimoto, T. and Miyake, C. (2011) Methylglyoxal functions as Hill oxidant and stimulates the photoreduction of O2 at photosystem I: a symptom of plant diabetes. Plant Cell Environ. 34: 1454–1464. Sato, S. and Yanagisawa, S. (2014) Characterization of metabolic states of Arabidopsis thaliana under diverse carbon and nitrogen nutrient conditions via targeted metabolomic analysis. Plant Cell Physiol. 55: 306–319. Sato, T., Maekawa, S., Yasuda, S., Domeki, Y., Sueyoshi, K., Fujiwara, M. et al. (2011) Identification of 14-3-3 proteins as a target of ATL31 ubiquitin ligase, a regulator of the C/N response in Arabidopsis. Plant J. 68: 137–146. Sato, T., Maekawa, S., Yasuda, S., Sonoda, Y., Katoh, E., Ichikawa, T. et al. (2009) CN1/ATL31, a RING-type ubiquitin ligase that functions in the carbon /nitrogen response for growth phase transition in Arabidopsis seedlings. Plant J. 60: 852–864. Takagi, D., Inoue, H., Odawara, M., Shimakawa, G. and Miyake, C. (2014) The Calvin cycle inevitably produces sugar-derived reactive carbonyl methylglyoxal during photosynthesis: A potential cause of plant diabetes. Plant Cell Physiol. 55: 333–340. Takatani, N., Ito, T., Kiba, T., Mori, M., Miyamoto, T., Maeda, S.-i. et al. (2014) Effects of high CO2 on growth and metabolism of Arabidopsis seedlings during growth with a constantly limited supply of nitrogen. Plant Cell Physiol. 55: 281–292. Terashima, I., Hanba, Y.T., Tazoe, Y., Vyas, P. and Yano, S. (2006) Irradiance and Phenotype: Comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp. Bot. 57: 343–354. Tsutsumi, K., Konno, M., Miyazawa, S-.I. and Miyao, M. (2014) Sites of action of elevated CO2 on leaf development in rice: Discrimination between the effects of elevated CO2 and nitrogen deficiency. Plant Cell Physiol. 55: 258–268. Watanabe, C.K., Sato, S., Yanagisawa, S., Uesono, Y., Terashima, I. and Noguchi, K. (2014) Effects of elevated CO2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and their diurnal patterns in Arabidopsis thaliana: Possible relationships with respiratory rates. Plant Cell Physiol. 55: 341–357. Yamazaki, K. (1963) Studies on the leaf formation in rice plants. I. Observation on the successive development in leaf formation. Jpn. J. Crop Sci. 341: 371–378.
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Hashimoto, M., Negi, J., Young, J., Israelsson, M., Schroeder, J.I. and Iba, K. (2006) Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat. Cell Biol. 8: 391–397. Hashimoto-Sugimoto, M., Higaki, T., Yaeno, T., Nagami, A., Irie, M., Fujimi, M. et al. (2013) A Munc13-like protein in Arabidopsis mediated H+-ATPase translocation that is essential for stomatal responses. Nat. Commun. 4: 2215. IPCC (2013) Summary for Policymakers. In Climate Change 2013: The Physical Science Basis, Edited by Stocker, T.F., Qin, D., Platter, G.-K., Tignor, M., Allen, S.K., Boschung, J. et al., pp.1–27, Cambridge Univ. Press, Cambridge. Kaneko, K., Inomata, T., Masui, T., Koshu, T., Umezawa, Y., Itoh, K. et al. (2014) Nucleotide pyrophosphatase/phosphodiesterase 1 exerts a negative effect on starch accumulation and growth in rice seedlings under high temperature and CO2 concentration conditions. Plant Cell Physiol. 55: 320–332. Kaneko, K., Yamada, C., Yanagida, A., Koshu, T., Umezawa, Y., Itoh, K. et al. (2011) Differential localizations and functions of rice nucleotide pyrophosphatase/phosphodiesterase isozymes 1 and 3. Plant Biotechnol. 28: 69 76. Keeling, C.D., Chin, J.F.S. and Whorf, T.P. (1996) Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382: 146–149. Kobayashi, K., Okada, M., Kim, H.Y., Lieffering, M., Miura, S. and Hasegawa, T. (2006) Paddy Rice Responses to Free-Air CO2 Enrichment. In Managed Ecosystems and CO2: Case Studies, Processes, and Perspectives. Edited by No¨sberger, J., Long, S.P., Norby, R.J., Stitt, M., Hendrey, G.R. and Blum, H. pp. 87–104. Springer, Berlin. Lake, J.A., Quick, W.P., Beerling, D.J. and Woodward, F.I. (2001) Signals from mature to new leave. Nature 411: 154–154. Leaky, A.D.B., Ainsworth, E.A., Bernacchi, C.J., Rogers, A., Long, S.P. and Ort, D.R. (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60: 2859–2876. Lopez, D., Venisse, J.-S., Fumanal, B., Chaumont, F., Guillot, E., Damoels, M.J. et al. (2013) Aquaporins and leaf hydraulics:Poplar shed new light. Plant Cell Physiol. 54: 1963–1975. Luo, Y., Hui, D. and Zhang, D. (2006) Elevated CO2 stimulated net accumulation of carbon and nitrogen in land ecosystems: a metaanalysis. Ecology 87: 53–63. Lu¨thi, D., Le Floch, M., Bereiter, B., Blunier, T., Barnola, J.-M., Siegenthaler, U. et al. (2008) High-resolution carbon dioxide concentration record 650,000-800,000 years before present. Nature 453: 379–382. Makino, A. and Mae, T. (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol. 40: 999–1006. Mori, I.C., Rhee, J., Shibasaka, M., Sasano, S., Kaneko, T., Horie, T. et al. (2014) CO2 transport by PIP2 aquaporins in barley. Plant Cell Physiol. 55: 251–257. Nanjo, Y., Oka, H., Ikarashi, N., Kaneko, K., Kitajima, A., Mitsui, T. et al. (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/ phosphodiesterase is transported from the ER-Golgi to the chloroplast through the secretory pathway. Plant Cell 18: 2582–2592. Negi, J., Hashimoto-Sugimoto, M., Kusumi, K. and Iba, K. (2014) New approaches to the biology of stomatal guard cells. Plant Cell Phyisol. 55: 241–250.
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan 3 Riken Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan *Corresponding author: E-mail, [email protected]; Fax: +81-3-5841-4465 2
Background
Downloaded from http://pcp.oxfordjournals.org/ at Mount Allison University on June 29, 2015
For the past 800,000 years, the atmospheric CO2 concentration, [CO2], has fluctuated between 180–200 and 250–280 ppmv during the different glacial and interglacial periods, respectively (Lu¨thi et al. 2008). Currently, we are in an interglacial period, where [CO2] had been around 280 ppmv for more than 10,000 years and up until the industrial revolution of the 1800s. Since then, [CO2] has been increasing with annual fluctuations peaking in winter, and the most recent peaks exceeding 400 ppmv. The increasing concentration rate has accelerated to the extent that atmospheric CO2 levels may reach twice those before the industrial revolution by the end of this century. This marked increase in [CO2] is the most influential cause of global warming (IPCC, 2013). Higher temperatures and increased [CO2] both pose serious problems to the environment and in particular to plants. This is because plants cannot keep pace with this rapid increase in [CO2] by means of adaptation alone, as most plants are adapted to an atmospheric [CO2] of below 300 ppmv. In 1957, Keeling and his group initiated continuous measurements of atmospheric [CO2] at the summit of Mauna Loa (e.g. Keeling et al. 1996), which continue to show an impressive increasing pattern of [CO2]. Stimulated by the importance of this issue, CO2 doubling growth experiments followed in the 1970s’. Arp (1991) meta-analysed the results of CO2 doubling experiments conducted up to 1990 and showed that enhancement of photosynthetic rates by high [CO2] was only observed in plants grown in very large pots or in fields. In experiments where plants were grown in small pots, photosynthesis was notably downregulated under high [CO2]; this phenomenon became known as the ‘pot size effect.’ From the mid 1990’s, large-scale experiments using open-top chambers or free air CO2 enrichment (FACE) systems were established to circumvent the pot size effect. The results of these large-scale experiments, however, still showed large variations even within the same species (e.g. Hasegawa et al. 2013) and clearly demonstrated that high [CO2] does not necessarily enhance plant growth or crop yield (Makino and Mae 1999, Ainsworth and Long 2005, Luo et al. 2006, Leakey et al. 2009). Thus the precise
effects of CO2 on plant growth and performance remain largely unknown. Because [CO2] will continue to rise for at least another several decades even according to the most optimistic predictions by the IPCC (2013), and because many plant functions are downregulated by high [CO2], it is vital that the detrimental effects of high [CO2] on plants are understood, and ways to overcome these effects sought. Since 2011, we have been running a five-year research project entitled ‘Comprehensive studies of plant responses to the high CO2 world by an innovative consortium of ecologists and molecular biologists’ supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT). In this special focus issue, some representative outputs from this consortium project have been compiled.
Stomata and mesophyll conductance It is widely known that in many angiosperm species the stomata close in response to high [CO2]. Several Arabidopsis thaliana mutants showing impaired stomatal responses to CO2 have been isolated using a high-throughput technique employing thermography of rosette leaves, and analysed (Hashimoto et al. 2006, Negi et al. 2008, Negi et al. 2013, HashimotoSugimoto et al. 2013). Negi et al. (2014) review these seminal studies. In addition, mobile water soluble signal(s) derived from the mesophyll of Commelina communis plants were shown to greatly accelerate guard cell responses to CO2 (Fujita et al. 2013), however, their identity remain unknown. Aquaporins have been implicated in regulating stomatal behaviour, mesophyll conductance for CO2 diffusion (Terashima et al. 2006), and leaf hydraulic conductance (Lopez et al. 2013). Although most studies so far have claimed that plasma membrane intrinsic protein 2 (PIP2)-type aquaporins are water channels, on pp. 251–257 Mori et al. (2014) clearly demonstrate that some barley (Hordeum vulgare) HvPIP2 aquaporins, including HvPIP2;1, act as CO2 channels, and identified the amino acid residue that is responsible for CO2 permeability. In addition, it was shown previously that overexpression of HvPIP2;1 in rice (Oryza sativa) increased mesophyll conductance for CO2 diffusion (Hanba et al. 2004). Thus, it would appear that some
Plant Cell Physiol. 55(2): 237–240 (2014) doi:10.1093/pcp/pcu022, available online at www.pcp.oxfordjournals.org ! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 55(2): 237–240 (2014) doi:10.1093/pcp/pcu022 ! The Author 2014.
237
aquaporins actually facilitate CO2 transfer and increase mesophyll conductance. In such cases, these aquaporins would be more appropriately called cooporins as previously proposed by Terashima et al. (2006). The next step would be to determine specific regulation mechanisms of leaf aquaporins and cooporins in a comprehensive manner.
C/N balance, Sato et al. (2009, 2011) identified the ubiquitin ligase CNI1/ATL31 as a novel C/N regulator. In these studies, C levels were manipulated with glucose or sucrose in the rooting medium. More recently, Aoyama et al. (2014), however, treated A. thaliana plants with high [CO2] instead of sugar and found that ATL31 is involved in promoting leaf senescence at high [CO2] and low N nutrition.
Plant development
C/N balance and the sink-source relationship At high [CO2] plants tend to accumulate sugar and decrease their nitrogen content, leading to a high C/N ratio in the plant body. Takatani et al. (2014), devised a unique experimental system with an A. thaliana mutant showing reduced nitrate uptake activity to study the nature of the C/N balance. At high [CO2] the mutant suffered from N stress when grown with nitrate, and exhibited some phenotypic features similar to those of wild-type plants subjected to N stress, such as a reduced shoot/root ratio, whereas metabolite levels remained unchanged even under high [CO2]. Thus this experimental system is an effective tool to help uncover plant response mechanisms to high [CO2]. In other work focusing on the
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Metabolism, respiration and translocation On pp. 306–319, Sato and Yanagisawa (2014) compares metabolite contents in A. thaliana grown with various concentrations of nitrate and/or ammonium and at various [CO2] and light levels. When N and light were sufficient, plant growth was enhanced with [CO2] up to 3600 ppmv, indicating A. thaliana’s potential to utilize CO2 at very high concentrations. It was also revealed that ammonium exerted drastic effects on metabolite patterns regardless of [CO2] levels. In a separate study using rice, Kaneko et al. assessed knockout mutants of nucleotide pyrophosphatase/ phosphodiesterase 1 (npp1) grown at high [CO2] and high temperatures. The results indicate that NPP1, a unique glycoprotein (Nanjo et al. 2006, Kaneko et al. 2011), exerts negative effects on growth and starch accumulation in plants grown at high [CO2] and high temperatures. Manipulation of NPP1 expression levels could potentially be a way to improve rice growth in the high CO2 era. On pp. 333–340, Takagi et al. (2014) show that methylglyoxal, a sugar-derived reactive carbonyl, was produced as a by-product of the triosephosphate isomerase reaction in the Calvin-Benson cycle in wheat (Triticum aestivum) chloroplasts and intact leaves. The production rate of methylglyoxal was dependent on light intensity and [CO2] and could lead to serious oxidative stress, called ‘plant diabetes’ (Saito et al. 2011). In the high CO2 era, it will be necessary to enhance protection mechanisms against this type of stress. Distinction of respiratory characteristics of A. thaliana shoots grown at 390 ppmv and those grown at 780 ppmv CO2 was the focus of a study by Watanabe et al. (2014). Respiration was limited by either substrate supply or demand for ATP in ATP-utilising reactions. At high [CO2], especially towards the end of the dark period, the rate of respiratory O2 uptake was limited by the demand for ATP, suggesting that respiration at high [CO2] tends to be limited by some anabolic processes. In this context, the alternative respiratory pathway may contribute to balancing the NAD(P)H/ATP ratio (Gandin et al. 2013). Duan et al. (2014) examined the impact of high [CO2] on sugar translocation systems in A. thaliana plants, such as abundance of plasmodesmata, and gene expression levels of the sucrose effluxer SWEET12 and sucrose transporters SUC2 and SUT4. They also examined the rates of assimilation and translocation using a 14CO2 tracer. The sugar translocation system changed considerably in response to high [CO2], with differences being observed between the first and third rosette leaves.
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Plant structural traits such as the shoot to root ratio, leaf thickness, and stomatal density can be modified at high [CO2]. Taking advantage of precise developmental studies of rice leaves (e.g. Yamazaki 1963), Tsutsumi et al. (2014) conducted a detailed developmental study employing transfer experiments, in which plants containing leaves at various developmental stages were transferred from ambient to high CO2 conditions. They succeeded in pinpointing the stages most sensitive to high [CO2] for various leaf morphological traits including leaf length, width, and blade thickness. Stomatal density and index, often reported to decrease at high [CO2] (e.g. Lake et al. 2001), were unchanged, however. These exciting results will form an invaluable basis for the future identification of factors responsible for these morphological and anatomical changes in response to high [CO2]. It is feasible that the shoot to root ratio may respond to changing [CO2], although some meta-analysis studies have not detected such tendencies (Poorter and Nagel, 2000). On pp. 269–280, Hachiya et al. (2014) analysed combined effects of low-medium pH and high CO2, or low nitrogen (N) stress and high [CO2] on growth of A. thaliana. The results clearly indicate that both of these combined conditions caused preferential root growth, but via different mechanisms. In low pH stress and high [CO2], accumulation of sugar caused a change in the auxin and cytokinin balance in a way that favors lateral root growth. Future experiments conducted under several growth conditions and with different relevant mutants (e.g. Hachiya et al. 2012) will be indispensable to further clarify mechanisms of changes in the shoot to root ratio in response to high [CO2].
These results highlight the plastic nature of the translocation system.
Rice FACE
Future scope Within this century, we will soon face a high CO2 era. It is highly likely that the majority of plants, which are adapted to an atmospheric [CO2] of below 300 ppmv, will suffer various detrimental effects. Thus, it is vital to continue research into this field, namely through large-scale growth experiments as well as precise molecular physiological studies, to clarify the respective mechanisms responsible for the various downregulations that occur under high CO2 conditions. Information gleaned from such studies could be used to optimize plant performance under various environmental conditions in a tailor-made manner, and generate valuable materials for breeding. To this aim, effective collaboration between ecologists, agronomists and molecular biologists is indispensable. Without these concerted efforts, we will not be able to increase biomass production, feed the 10 billion people estimated to populate the planet (Evans 1998), or maintain ecosystems that efficiently fix CO2 in the high CO2 era.
Funding This work and the studies compiled in this special issue were supported by a Grant-in-Aid for Scientific Research on Innovative Areas for “Comprehensive studies of plant responses to the high CO2 world by an innovative consortium of ecologists and molecular biologists.”
We thank professor Tomoyuki Yamaya, Editor-in-Chief of Plant and Cell Physiology, for providing us with the opportunity to showcase some of our work in this Special Focus Issue on Plant Response to CO2.
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In 1998, a team led by Kobayashi and Okada initiated the FACE project for paddy field rice (Kobayashi et al. 2006), and the lowcost light-weighted FACE facility operating in a pure CO2 injection mode developed by this team (Okada et al. 2001) has now been adopted in most FACE experiments using herbaceous plants. This team has been systematically producing data (e.g. Hasegawa et al. 2013) that will form a fundamental basis for sustainable rice production in the high CO2 era. Adachi et al. (2014) report the combined effects of high [CO2] and an increase in soil and water temperature by 2 C on rice production. High soil and water temperatures under high [CO2] accelerated downregulation or aging of the leaf photosynthetic capacity. In a different study, Chen et al. (2014) compared leaf photosynthetic properties between ambient and elevated [CO2] levels in a high-yielding indica variety (Takanari) and a popular japonica variety (Koshihikari). Takanari showed greater leaf photosynthesis and stomatal conductance as well as increased mesophyll conductance at both [CO2] levels. It is worth noting that leaf N on an area basis was not suppressed by high [CO2] in Takanari. These results indicate that Takanari will be an invaluable resource for rice breeding in the high CO2 era.
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