Growth and N Allocation in Rice Plants under CO2 Enrichment

Makino, Amane; Harada, Mikio; Satô, Tetsuya; Nakano, Hiromi; Mae, Tadahiko

doi:10.1104/pp.115.1.199

Cited by 91 publications

(64 citation statements)

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“…Nitrogen is highly invested in the photosynthetic machinery (18), and the leaf blade has a much higher nitrogen concentration than the leaf sheath and the root in rice plants (19). It is possible that the Osppc4 knockdown limits enlargement of the lamina area by suppressing nitrogen uptake or assimilation.…”

Section: Resultsmentioning

confidence: 99%

Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation

Masumoto

Miyazawa

Ohkawa

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

150

111

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Phosphoenolpyruvate carboxylase (PEPC) is a key enzyme of primary metabolism in bacteria, algae, and vascular plants, and is believed to be cytosolic. Here we show that rice (Oryza sativa L.) has a plant-type PEPC, Osppc4, that is targeted to the chloroplast. Osppc4 was expressed in all organs tested and showed high expression in the leaves. Its expression in the leaves was confined to mesophyll cells, and Osppc4 accounted for approximately one-third of total PEPC protein in the leaf blade. Recombinant Osppc4 was active in the PEPC reaction, showing V max comparable to cytosolic isozymes. Knockdown of Osppc4 expression by the RNAi technique resulted in stunting at the vegetative stage, which was much more marked when rice plants were grown with ammonium than with nitrate as the nitrogen source. Comparison of leaf metabolomes of ammonium-grown plants suggested that the knockdown suppressed ammonium assimilation and subsequent amino acid synthesis by reducing levels of organic acids, which are carbon skeleton donors for these processes. We also identified the chloroplastic PEPC gene in other Oryza species, all of which are adapted to waterlogged soil where the major nitrogen source is ammonium. This suggests that, in addition to glycolysis, the genus Oryza has a unique route to provide organic acids for ammonium assimilation that involves a chloroplastic PEPC, and that this route is crucial for growth with ammonium. This work provides evidence for diversity of primary ammonium assimilation in the leaves of vascular plants.amino acid synthesis | glycolysis | nitrogen assimilation | organic acid synthesis | Oryza

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Section: Resultsmentioning

confidence: 99%

Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation

Masumoto

Miyazawa

Ohkawa

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

150

111

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“…However, we believe that the physiological implications of the decrease in leaf N content are of crucial importance for the whole-plant growth under CO, enrichment. This decrease in leaf N content is not due to dilution of N caused by a relative increase in leaf area or plant biomass, because the decrease in leaf N is greater in plants grown with a low N supply, whereas the enhancement of the biomass is smaller at a low concentration of N. Further work aimed at resolving these problems will be presented in our companion paper (Makino et al, 1997).…”

Section: Lmplications Of a Decrease In Leaf Nmentioning

confidence: 99%

The Effect of Elevated Partial Pressures of CO2 on the Relationship between Photosynthetic Capacity and N Content in Rice Leaves

1997

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The effects of growth CO, levels on the photosynthetic rates; the amounts of ribulose-1,s-bisphosphate carboxylase (Rubisco), chlorophyll (Chl), and cytochrome fi sucrose phosphate synthase activity; and total N content were examined i n young, fully expanded leaves of rice (Oryza sativa 1.). l h e plants were grown hydroponically under two CO, partial pressures of 36 and 1 O0 Pa at three N concentrations. The light-saturated photosynthesis at 36 Pa CO, was lower i n the plants grown in 100 Pa CO, than those grown in 36 Pa CO,. Similarly, the amounts of Rubisco, Chl, and total N were decreased in the leaves of the plants grown in 100 Pa CO,. However, regression analysis showed no differences between the two CO, treatments in the relationship between photosynthesis and total N or i n the relationship between Rubisco and Chl and total N. Although a relative decrease in Rubisco to cytochrome f o r sucrose phosphate synthase was found i n the plants grown in 100 Pa C 0 2 , this was the result of a decrease in total N content by CO, enrichment. The activation state of Rubisco was also unaffected by growth CO, levels. Thus, decreases i n the photosynthetic capacity of the plants grown in 100 Pa CO, could be simply accounted for by a decrease in the absolute amount of leaf N. Leaf photosynthesis is affected by the levels of environmental CO, in which the plants are grown. Short-term (seconds to hours) CO, enrichment stimulates the photosynthetic rate per unit of leaf area. Plant mass is also enhanced during a subsequent long-term exposure (weeks to months) to elevated CO, levels. However, such a longterm CO, enrichment reduces the initial stimulation of photosynthesis and then frequently suppresses photosynthesis (for reviews, see Stitt, 1991; Bowes, 1993;Sage, 1994). These findings indicate that prolonged exposure to elevated CO, leads to changes in biochemical, physiological, or morphological factors, which remove or offset the initial stimulation of photosynthesis. However, the mechanisms of the suppression of photosynthesis by long-term CO, enrichment still remain unclear. Growth under high CO, partial pressures leads to carbohydrate accumulation. Since an apparent correlation between carbohydrate accumulation and the suppression of photosynthesis has often been reported (Sasek et al., 1985;Peet et al., 1986;Yelle et al., 1989;Wong, 1990;Xu et al., 1994), much attention has been paid to the causal relationship(s) between the two phenomena. Stitt (1991) proposed the existence of a feedback mechanism(s) by which the accumulation of carbohydrate indirectly leads to a decrease in the amounts of key components of the photosynthetic apparatus. In fact, many studies of long-term acclimation to elevated CO, partial pressures have shown a decrease in Rubisco (Peet et al., 1986;Sage et al., 1989; RowlandBamford et al., 1991;Xu et al., 1994; Jacob et al., 1995; Rogers et al., 1996). In addition, a decrease in the transcript levels of rbcS and rbcL mRNA was recently found in the plants grown at elevated CO, partial pressu...

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“…Acclimation to continuous light and elevated pCO 2 is typically characterized by a decline in the leaf carboxylation capacity and expression of Rubisco (Pilgrim and McClung, 1993;Drake et al, 1997), mediated by a negative feedback from the accumulation of sugars or starch (Dorais et al, 1996;Paul and Foyer, 2001). However, additional mechanisms do also seem to be important, particularly an alteration in the partitioning of nitrogen to leaves (Makino et al, 1997;Osborne et al, 1998). Based on these findings, we expected that photosynthesis in our experiment would be regulated by three key mechanisms, and we hypothesized that: 1) a decrease in the leaf carboxylation capacity underpins the acclimation of A to continuous illumination and elevated pCO 2 ; 2) that seasonal changes in the carboxylation capacity are linked to the accumulation of soluble sugars and/or starch in leaves during summer, particularly under pCO 2 enrichment; and 3) the seasonal suppression of photosynthetic capacity is additionally associated with a decrease in the partitioning of nitrogen to leaves.…”

mentioning

confidence: 99%

The Penalty of a Long, Hot Summer. Photosynthetic Acclimation to High CO2 and Continuous Light in “Living Fossil” Conifers

Osborne

Beerling

2003

Plant Physiology

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Deciduous forests covered the ice-free polar regions 280 to 40 million years ago under warm "greenhouse" climates and high atmospheric pCO 2 . Their deciduous habit is frequently interpreted as an adaptation for minimizing carbon losses during winter, but experiments with "living fossils" in a simulated warm polar environment refute this explanation. Measured carbon losses through leaf abscission of deciduous trees are significantly greater than losses through winter respiration in evergreens, yet annual rates of primary productivity are similar in all species. Here, we investigate mechanisms underlying this apparent paradox by measuring the seasonal patterns of leaf photosynthesis (A) under pCO 2 enrichment in the same trees. During spring, A increased significantly in coastal redwood (Sequoia sempervirens), dawn redwood (Metasequoia glyptostroboides), and swamp cypress (Taxodium distichum) at an elevated pCO 2 of 80 Pa compared with controls at 40 Pa. However, strong acclimation in Rubisco carboxylation capacity (V c,max ) completely offset the CO 2 response of A in all species by the end of 6 weeks of continuous illumination in the simulated polar summer. Further measurements demonstrated the temporary nature of acclimation, with increases in V c,max during autumn restoring the CO 2 sensitivity of A. Contrary to expectations, the acclimation of V c,max was not always accompanied by accumulation of leaf carbohydrates, but was associated with a decline in leaf nitrogen in summer, suggesting an alteration of the balance in plant sources and sinks for carbon and nitrogen. Preliminary calculations using A indicated that winter carbon losses through deciduous leaf abscission and respiration were recovered by 10 to 25 d of canopy carbon fixation during summer, thereby explaining the productivity paradox.Geological evidence shows that today's permanent polar ice sheets are a recent phenomenon, appearing some 34 million years ago (Ma) in Antarctica and 3 Ma in the Arctic (Zachos et al., 2001). Earlier periods of global warmth extending back to 280 Ma enabled forests to cover the polar regions and reach latitudes as high as 85°in both hemispheres (Spicer and Chapman, 1990). These ancient high latitude forests quite likely grew in an environment unlike any on Earth today, with mean winter temperatures above freezing (Pole and Macphail, 1996;Markwick, 1998; Tripati et al., 2001;Dutton et al., 2002), and an atmospheric pCO 2 enriched over current ambient levels (Royer et al., 2001). However, in common with modern polar vegetation, they would have experienced strong seasonality in daylength (Creber and Chaloner, 1985). For example, trees at a latitude of 69°are exposed to continuous sunlight for 6 weeks in the summer and an equal period of darkness in winter (Beerling and Osborne, 2002).Fossils suggest that polar forests were largely deciduous (Spicer and Chapman, 1990), and this is frequently interpreted as an adaptation for minimizing canopy respiration during the warm, dark polar winter (Chaney, 1947;Hickey, 1984; Wolfe...

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Growth and N Allocation in Rice Plants under CO2 Enrichment

Cited by 91 publications

References 18 publications

Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation

Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation

The Effect of Elevated Partial Pressures of CO2 on the Relationship between Photosynthetic Capacity and N Content in Rice Leaves

The Penalty of a Long, Hot Summer. Photosynthetic Acclimation to High CO2 and Continuous Light in “Living Fossil” Conifers

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