Senescence of Top Three Leaves in Field-Grown Rice Plants
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1 _ JOURNAL OF PLANT NUTRITION Vol. 26, No. 12, pp , 2003 Senescence of Top Three Leaves in Field-Grown Rice Plants Chufu Zhang, 1 Shaobing Peng, 2, * and Rebecca C. Laza 2 1 Key Laboratory of MOE for Plant Developmental Biology, School of Life Sciences, Wuhan University, Wuhan, The People s Republic of China 2 Crop, Soil and Water Sciences Division, International Rice Research Institute (IRRI), Metro Manila, Philippines ABSTRACT The top three leaves play important roles in biomass production and grain yield of rice (Oryza sativa L.) crop since the three leaves not only assimilate majority of carbon for grain filling during ripening phase, but also provide large proportion of remobilized-nitrogen (N) for grain development during their senescence. The objectives of this study were to (a) compare senescence of the top three leaves and (b) compare the changes in N, chlorophyll, and ribulose-1,5-bisphosphate carboxylase=oxygenase (Rubisco) contents of the top three leaves after their full expansion in field-grown rice plants. When the basis of comparison among the top three leaves was plant age in terms of days after transplanting (DAT), *Correspondence: Shaobing Peng, Crop, Soil and Water Sciences Division, International Rice Research Institute (IRRI), DAPO Box 7777, Metro Manila, Philippines; s.peng@cgiar.org DOI: =PLN Copyright # 2003 by Marcel Dekker, Inc (Print); (Online)
2 2454 Zhang, Peng, and Laza senescence generally started earliest in 3rd leaf, intermediate in 2nd leaf, and latest in flag leaf. If the basis of comparison among the top three leaves was leaf age in terms of days after full leaf expansion (DAFE), it was not clear which leaf senesced earlier. Senescence rate was generally greatest in flag leaf, intermediate in 2nd leaf, and smallest in 3rd leaf. Ribulose-1,5-bisphosphate carboxylase=oxygenase content declined earlier, and at a faster rate than N and chlorophyll contents during the senescence of all top three leaves. Correlation analysis indicated a close relationship between N and chlorophyll contents. Ribulose-1,5-bisphosphate carboxylase=oxygenase content correlated with N content better than with chlorophyll content. The suitability of N, chlorophyll, and Rubisco contents for quantifying the leaf senescence of field-grown rice plants is discussed. Key Words: Chlorophyll content; Leaf nitrogen content; Leaf senescence; Ribulose-1,5-bisphosphate carboxylase=oxygenase; Rice; Top three leaves. INTRODUCTION Leaf senescence in cereal crops is accompanied by two processes: decline in leaf photosynthetic rate and remobilization of nutrients. [1] In rice 60 90% of total carbon in the panicles at harvest is derived from photosynthesis after heading, while 80% or more of nitrogen (N) in the panicles at harvest is absorbed before heading and remobilized from vegetative organs. [2] Therefore, leaf senescence during reproductive and ripening stages is directly related to biomass production and grain yield of rice crop. [3] Ribulose-1,5-bisphosphate carboxylase=oxygenase (Rubisco, EC ) is a key enzyme in the photosynthetic fixation of CO 2 in green plants and is also the predominant leaf protein. [4] In rice plants, this protein accounts for more than 50% of the soluble leaf proteins and over 25% of the total leaf N. [5] During leaf senescence, specific carboxylase activity of Rubisco did not change and a decline in activity was caused by the reduction in the amount of Rubisco protein in rice plants. [6] Mae et al. [7] studied the changes in Rubisco content of 12th leaf (4th leaf counting from the top) during its life span in rice plants. The amount of Rubisco increased during leaf expansion and reached maximum a week after full expansion. Thereafter, it degraded at a faster rate during senescence than other soluble proteins. When the leaf senesced completely, it contained negligible Rubisco protein but about 30% of N still remained in the leaves of rice plants. During leaf senescence, chlorophyll content also declines but the rate of the decline is much slower than Rubisco content. [6,8] Single-leaf net photosynthetic rate (P n ) is closely
3 Senescence of Top Three Leaves in Rice Plants 2455 correlated with Rubisco content [6] and N content [9,10] in rice plants. The decline in P n is also correlated with loss of chlorophyll during leaf senescence. [11,12] Ribulose-1,5-bisphosphate carboxylase=oxygenase, N, and chlorophyll contents have often been used to quantify leaf senescence. [3,5,6,12] The top three leaves of rice plants contribute most to grain yield because the top three leaves (a) have the largest leaf area; (b) have the longest life span; and (c) their functional period coincides with panicle development and grain filling. [3,13] The top three leaves not only assimilate majority of carbon for grain filling during ripening phase, but also provide large proportion of remobilized-n for grain development during their senescence. [2] Changes in Rubisco, N, and chlorophyll contents of 4th (counting from the top) and flag leaves during leaf senescence have been studied intensively, [5,7,8] but most of these studies were conducted using hydroponically grown plants in pots under greenhouse conditions. Biswas and Choudhuri [14] and Ray et al. [3] compared leaf senescence of the top three leaves during the ripening period under field conditions. The comparison of leaf senescence among the top three leaves was based on plant age (from heading to maturity) in their studies. They reported that the flag leaf senesced earlier and faster than 2nd and 3rd leaves. In this study, comparison of leaf senescence among the top three leaves was based on leaf age (from full leaf expansion to near death) and plant age in terms of days after transplanting (DAT) in field-grown rice plants. The objectives were to (a) compare the timing and rate of senescence of the top three leaves of rice plants based on leaf age and plant age and (b) compare the changes in N, chlorophyll, and Rubisco contents of the top three leaves after their full expansion. MATERIALS AND METHODS Plant Materials Two rice genotypes (IR72 and IR ) were grown in the experimental farm of the International Rice Research Institute, Philippines in the dry season (January May) of 1997 in a randomized block design with four replications. Fourteen-day-old seedlings were transplanted on 9 January. Hill spacing was m with four seedlings per hill. Plot size was 5 6m. Plants received a total of 225 kg ha 1 of N in the form of urea. Nitrogen was applied at four different growth stages (60 kg at 1 d before transplanting, 60 kg at mid-tillering, 60 kg at panicle initiation, and 45 kg at flowering) to ensure N sufficiency throughout the entire growing period. Phosphorus (30 kg P ha 1 as single superphosphate), potassium (40 kg K ha 1 as KCl), and zinc (5 kg Zn ha 1 as zinc sulfate heptahydrate) were applied and incorporated in all plots 1 d before transplanting.
4 2456 Zhang, Peng, and Laza Seventy leaves per replication and per leaf position were tagged when 3rd, 2nd, and flag leaves on the main stems were fully expanded, respectively. Seven leaves per replication were detached every 6 8 days from 0 days after full expansion (DAFE) until near death when 90% of leaf blade turned to yellow and dried up (Table 1). Leaf samples were stored at 70 C before extraction. Extraction of Soluble Proteins Frozen plant material (0.5 g) was ground to a fine powder in a precooled mortar with sand and pestle after adding liquid N, and then homogenized in an extraction buffer [10 ml g 1 fresh weight (FW)] containing 50 mm Tris HCl (ph 7.8), 20 mm MgCl 2, 1.0 mm EDTA, 0.1% BSA, 10 mm 2-mercaptoethanol, 1.0 mm PMSF, and 5.0 mgml 1 leupeptin. [15] The homogenates were centrifuged at 20,000g for 20 min. The supernatants were stored at 70 C before assay. Isolation and Determination of Rubisco Protein Ribulose-1,5-bisphosphate carboxylase=oxygenase subunits were separated by SDS-PAGE. [16] Electrophoresis was done in a Bio-Rad Mini Protein II electrophoretic cell with 12.5% gel. The amount of each sample applied to Table 1. Sampling dates as indicated by DAFE and DAT of the top three leaves for the measurements of leaf senescence parameters. Flag leaf 2nd leaf 3rd leaf Sampling number DAFE DAT DAFE DAT DAFE DAT Note: The crop reached panicle initiation stage at 42 DAT and flowering stage at 71 DAT.
5 Senescence of Top Three Leaves in Rice Plants 2457 the slot of the gel was 15 ml. After electrophoresis, the bands of Rubisco subunit polypeptides were treated according to Makino et al. [17] The gel was stained with 0.25% (w=v) Comassie Brilliant Blue R-250 (CBB) in 45% (v=v) methanol and 10% (v=v) acetic acid at room temperature for 8 h with gentle shaking. The stained gel was first destained in 20% (v=v) methanol and 7% (v=v) acetic acid for 3 h, and then the destaining solution was renewed and a piece of tissue paper was immersed together with the gel in the destaining solution for absorbing the dyes. Overnight destaining was necessary with gentle shaking to make the gel background colorless. The stained bands of both large subunit and small subunit were cut out of the gel with a razor blade and eluted in 2.0 ml formamide in a capped test tube at 50 C for 5 h with shaking. The resultant solution was read at 595 nm with a spectrophotometer (Shimadzu UV-2201, Japan). Purified Rubisco from rice plants was used as the standard in determining the content of the protein. Determination of Chlorophyll and Nitrogen Chlorophyll was extracted from 50 mg leaf samples in 10.0 ml 80% acetone for 16 h in the dark and was determined spectrophotometrically at 652 nm. [18] The amount of chlorophyll in rice leaves was expressed as mg g 1 FW. Leaf N was analyzed with micro-kjeldahl method after the leaf samples were oven-dried at 70 C to constant weight. [19] Leaf N content was expressed as mg N g 1 dry weight (DW). Statistical Analysis Regression analysis between leaf senescence parameters and DAFE was done to determine the daily rate of senescence of top three leaves. The slope of the regression line represents the daily rate of leaf senescence. Regression equation was based on sampling number 3 7 for N and chlorophyll contents and on sampling number 2 7 for Rubisco content (Table 1). Comparison between the slopes of different leaf positions was based on t-test. [20] Correlation analysis was conducted among the leaf senescence parameters. RESULTS The two rice genotypes (IR72 and IR ) showed similar results in terms of changes in N, chlorophyll, and Rubisco contents of the top three leaves after their full expansion. Only data of IR72 are
6 2458 Zhang, Peng, and Laza presented in this paper. The top three leaves reached full expansion at different crop stages. The 3rd leaf was fully expanded when the crop was about 5 days after panicle initiation stage and the flag leaf reached full expansion around booting stage. The 2nd leaf was fully expanded midway between panicle initiation and booting stage. Consequently, the senescing phase of the top three leaves coincided with different stages of panicle and grain development. The duration from full expansion to near death when 90% of leaf blade turned to yellow and dried up was 6 7 days shorter in flag leaf than 2nd and 3rd leaves. Contents of N, chlorophyll, and Rubisco declined during senescence phase in all top three leaves (Fig. 1), which was evident by the fact that slopes were negative and significantly different from zero in all three senescence parameters for all three leaf positions (Table 2). The maximum N content of top three leaves was about 32 mg g 1 DW [Fig. l(a)]. Leaf N content declined to a minimum level of 6 mg g 1 over 50-days. Leaf N content started to decline at different DAFE across leaves. Nitrogen content of 3rd leaf declined earlier than the flag leaf, and the flag leaf declined earlier than 2nd leaf. The rate of decline in N content was significantly greater in flag and 2nd leaves than in 3rd leaf (Table 2). The maximum chlorophyll content of top three leaves reached 4.2 mg g 1 FW [Fig. l(b)]. It declined to as low as 0.2 mg g 1 FW. The 3rd leaf had significantly higher maximum chlorophyll content than flag leaf and 2nd leaf. The decline of 3rd leaf in chlorophyll content was earlier than flag leaf and 2nd leaf. The rate of decline in chlorophyll content was significantly greater in flag leaf than in 2nd and 3rd leaves (Table 2). The maximum Rubisco content of top three leaves reached 23 mg g 1 FW [Fig. 1(C)]. The Rubisco contents of all top three leaves were close to zero at crop maturity. The decline in Rubisco content was slightly earlier in 2nd leaf than in flag and 3rd leaves. However, the rate of decline in Rubisco content was significantly greater in flag leaf than in 2nd and 3rd leaves (Table 2). When the basis of comparison among the top three leaves was plant age in terms of DAT rather than leaf age, the decline in N content was earlier in 3rd leaf than in flag leaf and 2nd leaf [Fig. 2(A)]. The decline in chlorophyll content started earliest in 3rd leaf, intermediate in 2nd leaf, and latest in flag leaf [Fig. 2(B)]. Ribulose-1,5-bisphosphate carboxylase=oxygenase content of 2nd and 3rd leaves declined earlier than that of flag leaf [Fig. 3(C)]. In general, Rubisco content declined earlier than N and chlorophyll content (Fig. 3). The decline in N content was slightly earlier than chlorophyll content. Ribulose-1,5-bisphosphate carboxylase=oxygenase declined at a significantly faster rate than N and chlorophyll in all top three leaves from 7 to 28 DAFE. The rate of decline in chlorophyll content was slightly slower than in N content over the same period. On average, there was 71.7%, 80.9%, and
7 Senescence of Top Three Leaves in Rice Plants 2459 Figure 1. Comparison among the top three leaves on the main stems of field-grown IR72 in leaf nitrogen (A), chlorophyll (B), Rubisco (C) contents based on leaf age in terms of DAFE. Chlorophyll and Rubisco contents were expressed on FW basis, while nitrogen content was on DW basis. Vertical bars represent one standard error of the mean and are smaller than the data points in some cases.
8 2460 Zhang, Peng, and Laza Table 2. Regression analysis between leaf senescence parameters and DAFE of the top three leaves. Leaf position Slope Intercept Sample size Coefficient of determination Nitrogen content Flag leaf 0.62 a* nd leaf 0.63 a rd leaf 0.46 b Chlorophyll content Flag leaf a nd leaf b rd leaf b Rubisco content Flag leaf 0.69 a nd leaf 0.52 b rd leaf 0.51 b Note: The slope of the regression line represents the daily rate of leaf senescence. Regression equation was based on sampling number 3 7 for N and chlorophyll contents and on sampling number 2 7 for Rubisco content (see Table 1). Sample size is equal to the number of sampling four replications. *Within each senescence parameter, slopes followed by different letters are significantly different at 0.05 probability level according to t-test. 99.6% reduction in N, chlorophyll, and Rubisco contents, respectively during the senescence of the top three leaves. Overall, the decline patterns of N and chlorophyll were relatively similar but very different from the decline pattern of Rubisco. Chlorophyll content was highly correlated with N content [Fig. 4(A)]. This was true for all top three leaves. However, the correlation between chlorophyll and N content was leaf-age dependent with correlation coefficient (r) of 0.34 at 0 20 DAFE and 0.98 at DAFE (data not shown). Ribulose-1,5-bisphosphate carboxylase=oxygenase content was also significantly correlated with N content [Fig. 4(B)]. Nitrogen content had slightly closer relationship with chlorophyll content than with Rubisco content. When the Rubisco content approached 0 mg g 1 FW, there was still 6 to 12 mg N g 1 DW in the top three leaves. The correlation between Rubisco and chlorophyll content was relatively weak [Fig. 4(C)]. Leaf age also affected the relationship of Rubisco contents with N and chlorophyll contents with much stronger correlation at DAFE than at 0 20 DAFE (data not shown). In general,
9 Senescence of Top Three Leaves in Rice Plants 2461 Figure 2. Comparison among the top three leaves on the main stems of field-grown IR72 in leaf nitrogen (A), chlorophyll (B), Rubisco (C) contents based on plant age in terms of DAT. Chlorophyll and Rubisco contents were expressed on FW basis, while nitrogen content was on DW basis. Vertical bars represent one standard error of the mean and are smaller than the data points in some cases.
10 2462 Zhang, Peng, and Laza Figure 3. Comparison among changes in leaf nitrogen, chlorophyll, Rubisco contents of flag leaf (A), 2nd leaf (B) and 3rd leaf (C) on the main stems of field-grown IR72 from full leaf expansion through senescence. Nitrogen, chlorophyll, and Rubisco were expressed as the percentage of their maximum, respectively.
11 Senescence of Top Three Leaves in Rice Plants 2463 Figure 4. Relationship between chlorophyll and N contents (A), between Rubisco and nitrogen contents (B), and between Rubisco and chlorophyll contents (C) of the top three leaves on the main stems of field-grown IR72 from full leaf expansion through senescence.
12 2464 Zhang, Peng, and Laza the correlations among leaf N, chlorophyll, and Rubisco contents were similar in the top three leaves. DISCUSSION When the basis of comparison among the top three leaves was leaf age in terms of DAFE, it was not clear which leaf senesced earlier because the differences in the timing of decline among the top three leaves were inconsistent across the three senescence parameters. However, if the basis of comparison among the top three leaves was plant age in terms of DAT rather than leaf age, senescence generally started earliest in 3rd leaf, intermediate in 2nd leaf, and latest in flag leaf. This conclusion contradicted the findings of Biswas and Choudhuri [14] and Ray et al. [3] They reported that the flag leaf of cultivar Jaya senesced earlier than 2nd and 3rd leaves during grain filling period. This contradiction might be due to the fact that leaf senescence was monitored during different life span of leaves in the two studies. In this study, leaf senescence was measured starting from full expansion until near death, while Biswas and Choudhuri [14] monitored leaf senescence from heading to harvest. When all three senescence parameters were considered, the rate of leaf senescence was generally greatest in flag leaf, intermediate in 2nd leaf, and smallest in 3rd leaf. This is consistent with the findings of Biswas and Choudhuri [14] and Ray et al. [3] They reported that the flag leaf of cultivar Jaya senesced faster than 2nd and 3rd leaves during grain filling period. The maximum value of Rubisco content in this study is comparable with previous reports. [6,21] However, maximum chlorophyll content of this study is about 50% greater than that reported by Makino et al. [6] This might be due to differences in genotypes and growing conditions between the two studies. Ribulose-1,5-bisphosphate carboxylase=oxygenase content declined earlier than N and chlorophyll content during the senescence of all top three leaves. The rate of decline was much faster in Rubisco than in N and chlorophyll. This is consistent with the results of Makino et al. [6] and Ladha et al. [8] The pattern of decline in N content during leaf senescence was similar to that of chlorophyll content, although the decline in N content was slightly earlier than chlorophyll. Correlation analysis indicated a close relationship between leaf N and chlorophyll content. Ribulose-1,5-bisphosphate carboxylase=oxygenase content correlated with N content better than with chlorophyll content. At issue is which parameter is the most suitable indicator of leaf senescence in field-grown rice plants. The question could not be addressed
13 Senescence of Top Three Leaves in Rice Plants 2465 here directly since P n was not measured in this study because of variable solar radiation during the experimental period. Camp et al. [11] found that Rubisco content decreased at a much faster rate than P n during leaf senescence. Field data indicated that photosynthetic capacity remained significant when leaf Rubisco content approached zero (Murchie, personal communication). Tsunoda [22] stated that leaf N content correlated better with P n than Rubisco content. It was speculated that this could be due to the fact that leaf N can be measured more accurately than Rubisco content. [23] Chlorophyll content seldom limits P n under sufficient PAR [24] because more chlorophyll is contained in an ordinary leaf than necessary. Under low PAR, however, chlorophyll content may limit P n since the rate of light reaction may limit the overall process of photosynthesis. [25] In rice, chlorophyll content is closely correlated with N concentration, so an apparent close relationship exists between chlorophyll content and P n. [23] However, if the variation in chlorophyll content is caused by different genotypes or by other nutrients such as phosphorus or potassium, chlorophyll content is no longer correlated with P n. [26] Makino et al. [6] reported that loss of chlorophyll during leaf senescence did not necessarily indicate the decrease in photosynthetic activity. Kura-Hotta et al. [12] found that photosynthetic capacity decreased more rapidly than chlorophyll content during leaf senescence. Close correlation between leaf N content and P n has been reported in many studies, regardless of plant age or leaf age. [9,10,27] These studies suggest that leaf N content related to P n more closely than chlorophyll and Rubisco contents during leaf senescence and leaf N content could be a better indicator of leaf senescence compared with chlorophyll and Rubisco contents. In this experiment, coefficient of variation (CV) across four replications was 7.7%, 8.4%, and 16.0% for the measurements of leaf N, chlorophyll, and Rubisco contents, respectively. This variation accounted for the differences of leaf samples taken in the four replications and errors during measurement procedures in the laboratory. The determination of leaf N and chlorophyll is relatively simple compared with Rubisco measurement. Furthermore, leaf N content is measured using dry leaf tissues whereas chlorophyll and Rubisco contents are measured with fresh leaf tissues. Dry leaf tissues can be stored at least for 2 years without any change in N content. [28] Therefore, for quantifying leaf senescence of field-grown rice plants in a screening program where large number of samples is involved, leaf N content could be a more preferred parameter than Rubisco or chlorophyll contents. In conclusion, senescence generally started earliest in 3rd leaf, intermediate in 2nd leaf, and latest in flag leaf based on plant age. If the basis of comparison among the top three leaves was leaf age, it was not clear which leaf senesced earlier. Senescence rate was generally greatest in flag leaf, intermediate in 2nd leaf, and smallest in 3rd leaf. Ribulose-1,5-bisphosphate
14 2466 Zhang, Peng, and Laza carboxylase=oxygenase content declined earlier and faster than N and chlorophyll during the senescence of all top three leaves. Considering both precision and convenience of measurement, leaf N content is more practical than chlorophyll and Rubisco contents in quantifying leaf senescence of rice plants in field experiments. ACKNOWLEDGMENTS This project was partially supported by the National Natural Science Foundation of China (Project No ). REFERENCES 1. Mae, T.; Ohiro, K. The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol. 1981, 22, Mae, T. Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis, and yield potential. Plant Soil 1997, 196, Ray, S.; Mondal, W.A.; Choudhuri, M.A. Regulation of leaf senescence, grain-filling and yield of rice by kinetin and abscisic acid. Physiol. Plant. 1983, 59, Ellis, R.J. The most abundant protein in the world. Trends Biochem. Sci. 1979, 4, Makino, A.; Mae, T.; Ohiro, K. Relation between nitrogen and ribulose- 1,5-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant Cell Physiol. 1984, 25, Makino, A.; Mae, T.; Ohiro, K. Photosynthesis and ribulose-1,5-bisphosphate carboxylase in rice leaves: changes in photosynthesis and enzymes involved in carbon assimilation from leaf development through senescence. Plant Physiol. 1983, 73, Mae, T.; Makino, A.; Ohiro, K. Changes in the amount of ribulose bisphosphate carboxylase synthesized and degraded during the life span of rice leaf (Oryza sativa L.). Plant Cell Physiol. 1983, 24, Ladha, J.K.; Kirk, G.J.D.; Bennett, J.; Peng, S.; Reddy, C.K.; Reddy, P.M.; Singh, U. Opportunities for increased nitrogen-use efficiency from improved lowland rice germplasm. Field Crops Res. 1998, 56, Yoshida, S.; Coronel, V. Nitrogen nutrition, leaf resistance, and leaf photosynthetic rate of the rice plant. Soil Sci. Plant Nutr. 1976, 22,
15 Senescence of Top Three Leaves in Rice Plants Peng, S.; Cassman, K.G.; Kropff, M.J. Relationship between leaf photosynthesis and nitrogen content of field-grown rice in the tropics. Crop Sci. 1995, 35, Camp, P.J.; Huber, S.C.; Burke, J.J.; Moreland, D.E. Biochemical changes that occur during senescence of wheat leaves. Plant Physiol. 1982, 70, Kura-Hotta, M.; Satoh, K.; Katoh, S. Relationship between photosynthesis and chlorophyll content during leaf senescence of rice seedlings. Plant Cell Physiol. 1987, 28, Yoshida, S. Fundamentals of Rice Crop Science; International Rice Research Institute: Manila, Philippines, Biswas, A.K.; Choudhuri, M.A. Differential behaviour of the flag leaf of intact rice plant during aging. Biochem. Physiol. Pflanzen 1978, 173, Martín del Molino, L.M.; Martínez-Carrasco, R.; Pérez, P.; Hernández, L.; Morcuende, R.; Sanchez de la Puente, L. Influence of nitrogen supply and sink strength on changes in leaf nitrogen compounds during senescence in two wheat cultivars. Physiol. Plant. 1995, 95, Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T 4. Nature 1970, 227, Makino, A.; Mae, T.; Ohiro, K. Colorimetric measurement of protein stained with coomassie brilliant blue R on sodium dodecyl sulfatepolyacrylamide gel electrophoresis by eluting with formamide. Agric. Biol. Chem. 1986, 50, Arnon, D.L. Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol. 1949, 24, Bremner, J.M.; Mulvaney, C.S. Nitrogen. In Methods of Soil Analysis, Part 2; Page, A.L., Miller, R.H., Keeney, D.R., Eds.; Amer. Soc. Agron.: Madison, WI, 1982; SAS Institute. SAS User s Guide: Statistics, 4th Ed.; SAS Institute: Cary, NC, Makino, A.; Mae, T.; Ohiro, K. Changes in photosynthetic capacity in rice leaves from emergence through senescence: analysis from ribulose-1,5- bisphosphate carboxylase and leaf senescence. Plant Cell Physiol. 1984, 25, Tsunoda, S. Photosynthetic efficiency in rice and wheat. In Rice Breeding; International Rice Research Institute: Manila, Philippines, 1972; Peng, S. Single-leaf and canopy photosynthesis of rice. In Redesigning Rice Photosynthesis to Increase Yield; Sheehy, J.E., Mitchell, P.L., Hardy, B., Eds.; International Rice Research Institute: Manila, Philippines and Elsevier Science: Amsterdam, The Netherlands, 2000; Rabinowitch, E.I. Photosynthesis and Related Processes; Interscience Publishers, Inc.: New York, 1956.
16 2468 Zhang, Peng, and Laza 25. Murata, Y. Photosynthesis, respiration, and nitrogen response. In The Mineral Nutrition of the Rice Plant; Johns-Hopkins Press: Baltimore, MD, 1965; Yoshida, S.; Nakabayashi, K.; Perez, P.H. Photosynthesis of the Rice Plant; International Rice Research Institute: Manila, Philippines, Makino, A.; Mae, T.; Ohiro, K. Differences between wheat and rice in the enzymatic properties of ribulose-1,5-bisphosphate carboxylase=oxygenase and the relationship to photosynthetic gas exchange. Planta 1988, 174, Huang, J.; Peng, S. Storage methods and duration of plant tissues for total nitrogen analysis in rice leaves. Commun. Soil Sci. Plant Anal. 2004, 35, in press.
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