Tifway 419 Tifway-419 Tif-way 419 Chl a+b total porphyrin Chlide a+b Phe a+b Tifway nm 750 nm NDVI 680 NDVI 705 NDVI broad Chl a Chl b Car

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1 Tifway 419 Tifway-419 Tif-way 419 Chl a+b total porphyrin Chlide a+b Phe a+b Tifway nm 75 nm NDVI 68 NDVI 75 NDVI broad Chl a Chl b Car R 2.7 (p <.1) Chl b (phytol chain) NDVI LP Car MP Car NDVI (thylakoid membrane) NDVI (stroma) NDVI chlorophyll (Chl) chlorophyllide (Chlide) pheophytin (Phe) pheophorbide (Pho) Porphyrin IX protoporphyrin IX (PPIX) IX magnesium protoporphyrin IX (MGPP) protochlorophyllide (Pchlide) carotenoid (Car) less polar carotenoid (LP Car) more polar carotenoid (MP Car) dephytylated or nonesterified pigment phytylated or esterified pigment

2 Nitrogen Rate and Mowing Frequency Effects on Spectral Reflectance of Bermudagrass Tifway 419 (Cynodon transvaalensis x C. dactylon) Hung-Ming Chen 1, Ming-Huang Hsu 2, Zhi-Wei Yang 1, Wen-Dar Huang 1, Chi-Ming Yang 2*, and Shin-Shinge Chang 1* 1 Department of Agronomy, National Taiwan University, Taipei, Taiwan, R.O.C. 2 Research Center for Biodiversity, Academia Sinica, Nankang, Taipei, Taiwan, R.O.C. *Corresponding author: cmyang@gate.sinica.edu.tw, changss@ntu.edu.tw ABSTRACT: The objectives of this study were conducted to examine the contents of pigments in the leaves and vegetation reflectance spectrum of bermudagrass Tifway 419 (Cynodon transvaalensis x C. dactylon) with different nitrogen application rates and mowing frequencies. The contents of chlorophyll (Chl), its biosynthetic and degradative intermediates (total porphyrin; chlorophyllide, Chlide; pheophytin, Phe; phytylated and dephytylated pigments), and carotenoids in the leaves of bermudagrass Tifway 419 elevated with increasing nitrogen rates. The mole percents of three porphyrins (protoporphyrin, PPIX; magnesium protoporphyrin IX, MGPP; protochlorophyllide, Pchlide) were not influenced by nitrogen application rate significantly. The canopy reflectance spectra of bermudagrass Tifway 419 were measured. The reflectance in the range of 4 to 7 nm was very low, while near-infrared (NIR) band above 75 nm was very high. The reflectance in the near-infrared wavebands was increased with increasing nitrogen application rate, but the reflectance in the visible region was decreased as nitrogen application rate increased. Spectral indices NDVI 68, NDVI 75, and NDVI broad calculated using broad-band reflectance were correlated well with the contents of Chl a, Chl b, and Car (R 2 about.7, p <.1). The chlorophyll-related compounds containing phytol chain greatly contributed to changes in NDVI than those compounds without phytol chain, except for Chl b. The LP Car also played a more important role in NDVI change than the MP Car. Results suggest that NDVI calculated from vegetation reflectance spectra was more affected by the chlorophyll- and carotenoid-related compounds located onto the thylakoid membranes than those located in the stroma of chloroplast. Key words: Bermudagrass, Chlorophyll, Carotenoid, Reflectance spectra, Vegetation index.

3 (warm season grass) (Green) 328 (Bermudagrass Tifgreen 328) (Tifdwarf) (Tee) (Fairway) 328 (Bermudagrass Tifgreen 328) 419(Bermudagrass Tifway 419) (Zoysia spp.) (Eremochloa ophiuroides) ( 26) ( 2) (Huete, 1987; Maas, 1998) (leaf area index, LAI) (Pollock and Kanemasu, 1979; Gardner and Blad, 1986; Peterson et al., 1987) (Thomas and Gausman, 1977; Ercoli et al., 1993) (Al-Abbas et al., 1974; Milton et al., 1989; Milton et al., 1991; Adams et al., 1993; Blackmer et al., 1996) ( 1998) (Kruse, 24)

4 14 17 Tifway 419(Cynodon transvaalensis x C. dactylon) g m -2 N-P-K (slow release fertilizer) 12 mm 2 m 2 m Tifway 419 PPIX MGPP Pchlide Chl a Chl b Chlide a Chlide b Phe a Phe b (phytylated pigments) (dephytylated pigments) Car LP Car MP Car Yang et al. (1998) % 4,5 rpm 5 Hitachi U-2 A A A 44.5 a (Chlorophyll a Chl a) b (Chlorophyll b Chl b) (Carotenoid Car) Porra et al. (1989) a b Holm (1954) Chlorophyllide Pheophorbide A 661 (Phytol) (Nonesterified Dephytylated pigments) Chlorophyllide (Chlide) Pheophorbide (Pho)

5 4. Esterified (Phytylated) A 666 (Esterified Phytylated pigments) (Chlorophyll, Chl) Pheophytin (Phe) 5. PPIX MGPP Pchlide A 575 A 59 A 628 Protoporphyrin IX (PPIX) Mg-protoporphyrin IX (MGPP) Protochlorophyllide (Pchlide) Kahn et al. (1976) 6. Chlorophyllide a b (Chlide a b) A 667 A 65 Chlide a Chlide b Chlorophyllase (McFeeters et al., 1971) Chlide a Chlide b Beer-Lamba 7. A 44.5 (More polar carotenoid MP Car) Holm Porra MP Car 8. 8% 5 L 12.5% HCl A A A 47 A A Pheophytin a (Phe a) Pheophytin b (Phe b) A 47 (Less polar carotenoid LP Car) (Lichtenthaler, 1987) (model LI-18, LI-COR Inc., USA) 3 11 nm 1 nm m 2 ND 68 R 68 R 75 ND 68 = (R 75 -R 68 )/(R 75 +R 68 ) ND 75 R 75 R 75 ND 75 = (R 75 -R 75 )/(R 75 +R 75 ) ND broad SPOT NDVI Red nm NIR nm (Hsu et al., 23b) Tifway-419

6 NDVI 68 NDVI 75 NDVI broad NDVI Deng (1982, 1989) 1 (mean value normalization): n 1 X = x( k), n 1 k = * x(1) x(2) x(3) x( k) x = (,,,..., ) X X X X 2 (grey relational coefficient) γ γ(x (k), x j (k)) = min min max max x ( k) x j ( k) + ζ x ( k) x j ( k) j k j k max max x ( k) x j ( k) + ζ x ( k) x j ( k) j k j = 1,, m; k = 1,, n j (identification coefficient), [,1] x (reference data series) x j (test data series) x ( k) x j ( k) x (k) x j (k) min min j k x ( k) x j ( k) j (the secondary minimum difference) min x ( k) x j ( k) k k (the first minimum difference) max max * 3 )) γ ( x ( k), x ( k n * 1 γ ( x ( k), x j ( k)) = γ ( x ( k), x j ( k)) n 1 k = j 4 (grey relational order or grey order)

7 Tifway 419 Chl Chl 4,558 11,221 µg g -1 Chl 4,97 8,531 µg g -1 Chl ( 1A) Chl a/b ( 1B) Chl ( 2A) 693 nmole g -1 1,664 nmole g nmole g -1 1,278 nmole g -1 (mole percent of porphyrins) PPIX MGPP Pchlide 78% 22% % ( 2B 2C 2D) Chlide a+b Chlide a/b 5 g m -2 Chlide a+b Chlide a/b ( 3) Phe a+b 1,236 3,194 µg g -1 1,57 2,192 µg g -1 ( 4A) Phe a/b 2.3 ( 4B) Chl Phe Chlide Pho (Shioi and Sasa, 1986) Chl ( 5) Car ( 6A) Car 2,227 4,37 µg g -1 Car 2,12 3,698 µg g -1 Car/Chl Car/Chl.49.38

8 ( 6B) LP Car MP Car ( 7) Tifway 419 Chl a+b total porphyrin Chlide a+b Phe a+b Tifway 419 Chl a/b 3 Chl a/b Chl a/b Chl a Chl b Chl a ( ) Chl b Chl a ( ) Chl b Chl Chl Pho chlorophyllase (phytol chain) Chlide Pho Mg-dechelatase Phe Pho (Hendry et al., 1987; Matile et al., 1996) Chlide a/b Phe a/b Chl a Chl a Chlide a Pho a Chl b Chl b Chlide b Pho b Chl a/b ( 1B) PPIX MGPP MGPP Pchlide MGPP MGPP Pchlide Pchlide PPIX MGPP Pchlide (Hsu et al., 23a) (Hsu et al., 1995; Chen et al., 1996) Tifway nm 55 nm 7 nm 75 nm ( 8)

9 Tifway nm 69 nm (Gitelson and Merzlyak, 1994a, 1996) ( 8) ( 9) g m -2 7 nm (red edge) g m -2 7 nm ( 9) 5 nm 68 nm 5 nm 68 nm (Gitelson and Merzlyak, 1994a) 7 nm (blue-shift of red edge) NDVI Chl a Chl b Car 1 R NIR R 75 R Red R 68 NDVI 68 ( 1A) R 75 NDVI 75 ( 1B) SPOT (broad-band) NDVI broad Chl a Chl b Car 1C NDVI 68 NDVI 75 NDVI broad Chl a Chl b Car R 2.7 p <.1 68 nm (Chappelle et al., 1992; Thomas and Gausman, 1977) 75 nm (sensitivity) 75 nm NDVI (Gitelson and Merzlyak, 1994a, 1994b, 1996, 1997; Hsu et al., 23b) SPOT NDVI (Hsu et al., 23b; Huang et al., 25) NDVI 68 NDVI 75 NDVI broad

10 Chl a Chl b Car R 2.7 NDVI Chl a Chl b Car R 2.85 (Hsu et al., 23b; Huang et al., 25) (biomass) Car Chl (Oelmullar and Mohr, 1985) Car Chl (Mayfield and Taylor, 1984) Tifway 419 Car Chl Chl Car Chl Chl a Chl b Car NDVI Tifway 419 NDVI 68 NDVI 75 NDVI broad NDVI NDVI 68 NDVI 75 NDVI broad ( 1) NDVI 68 Car Chl a phytylated LP Car Phe b Phe a PPIX Dephytylated MP Car Chl b MGPP Chlide b Chlide a Pchlide NDVI 75 : Car LP Car Phytylated Chl a Phe b Phe a PPIX Dephytylated MP Car Chl b MGPP Chlide b Chlide a Pchlide NDVI broad : Car Chl a Phytylated LP Car Phe a Phe b PPIX Dephytylated MP Car MGPP Chl b Chlide b Chlide a Pchlide ( ) PPIX MGPP Pchlide Chl a Chl b Chlide a Chlide b Phe a Phe b phytylated dephytylated Car LP Car MP Car NDVI 68 NDVI 75 NDVI broad ( ) NDVI PPIX MGPP Pchlide Chlide a Chlide b (phytol chain) Chl a Chl b Phe a Phe

11 b NDVI (21) NDVI NDVI NDVI NDVI (Hsu et al., 23c) Chl b NDVI Chl b

12 1. 2 pp SPOT 5: (Oryza sativa L.) Adams, M.L., W.A. Norvell, J.H. Peverly, and W.D. Philpot Fluorescence and reflectance characteristics of manganese deficient soybean leaves: Effect of leaf age and choice of leaflet. Plant Soil : Al-Abbas, A.H., R. Barr, J.D. Hall, F.L. Crane, and M.F. Baumgardner Spectra of normal and nutrient-deficient maize leaves. Agron. J. 66: Blackmer, T.M., J.S. Schepers, G.E. Varvel, and E.A. Walter-Shea Nitrogen deficiency detection using reflected shortwave radiation from irrigated corn canopies. Agron. J. 88: Chappelle, E.W., M.S. Kim, and J.E. McMurtrey, III Ratio analysis of reflectance spectra (RARS): An algorithm for the remote estimation of the concentrations of chlorophyll a chlorophyll b, and carotenoids in soybean leaves. Remote Sens. Environ. 39: Chen, H.Y., Y.K. Lu, C.H. Chou, and C.M. Yang Analysis of pigment degradation in exocarp of papaya during late ripening. J. Chinese Agric. Chem. Soc. 34: Deng, J.L Control problems of grey systems. Systems Control Lett. 5: Deng, J.L Introduction to grey system theory. J. Grey System 1: Ercoli, L., M. Mariotti, A. Masoni, and F. Massantini Relationship between nitrogen and chlorophyll content and spectral properties in corn leaves. Eur. J. Agron. 2: Gardner, B.R., and B.L. Blad Evaluation of spectral reflectance models to estimate corn leaf area while minimizing the influence of soil background effect. Remote Sens. Environ. 2: Gitelson, A.A., and M.N. Merzlyak. 1994a. Spectral reflectance changes associated with autumn senescence of Aesculus hippocastanum L. and Acer platanoides L. leaves. Spectral features and relation to chlorophyll estimation. J.

13 Plant Physiol. 143: Gitelson, A.A., and M.N. Merzlyak. 1994b. Quantitative estimation of Chlorophyll a using reflectance spectra: Experiments with autumn chestnut and maple leaves. J. Photochem. Photobiol. (B) 22: Gitelson, A.A., and M.N. Merzlyak Signature analysis of leaf reflectance spectra: algorithm development for remote sensing of chlorophyll. J. Plant Physiol. 148: Gitelson, A.A., and M.N. Merzlyak Remote estimation of chlorophyll content in higher plant leaves. Intl. J. Remote Sens. 18: Hendry, G.A.F., J.D. Houghton, and S.B. Brown The degradation of chlorophyll a biological enigma. New Phytol. 17: Holm, G Chlorophyll mutations in barley. Acta Agric. Scand. 4: Hsu, J.C., Y.K. Lu, and C.M. Yang Analysis on pigments in the exocarp of orange fruit. Taiwania 4: Hsu, M.H., W.D. Huang, Z.W. Yang, Y.Z. Tsai, C.M. Yang, and S.S. Chang. 23a. Study on the chlorophyll biosynthetic and degradative pathway in the leaves of three sweet potatoes. Chinese Agron. J. 13: Hsu, M.H., W.D. Huang, Z.W. Yang, Y.Z. Ysai, S.S. Chang, and C.M. Yang. 23b. Remote estimation of pigment content in sweet potato leaves by reflectance spectra. Chinese Agron. J. 13: Hsu, M.H., W.D. Huang, Z.W. Yang, Y.Z. Tsai, S.S. Chang, J.S. Yang, and C.M. Yang. 23c. Grey relational analysis on the pigment contents and normalized difference vegetation index (NDVI) of sweet potato leaves. Chinese Agron. J. 13: Huang, W.D., M.H. Hsu, Z.W. Yang, J.C. Chen, Y.Z. Tsai, S.S. Chang, and C.M. Yang. 25 Mimicking satellite remote sensing of chlorophyll content in sugarcane (Saccharum officinarum) leaves. Crop Environ. Bioinformatics 2: Huete, A.R Soil dependent spectral response in a developing plant canopy. Agron. J. 79: Kahn, V.M., N. Avivi-Bieise and Wettstein, D. von Genetic regulation of chlorophyll synthesis analyzed with double mutants in barley. In: Genetics and Biogenesis of Chloroplasts and Mitochondria. (ed. by Bhuchler, T.). pp Elsevier/North-Holland Biomedical Press, Amsterdam. 27. Kruse, J., N. Christians, and M. Chaplin. 24. Remote Sensing Making your job a little easier with new technology. Grounds Maint. G Lichtenthaler, H.K Chlorophylls and carotenoids: pigments of photosynthetic biomembrane. Methods Enzymol. 148:

14 29. Maas, S.J Estimating cotton canopy ground cover from remotely sensed scene reflectance. Agron. J. 9: Matile, P., S. Hortensteiner, H. Thomas, and B. Krautler Chlorophyll breakdown in senescent leaves. Plant Physiol. 112: Mayfield, S.P., and W.C. Taylor Carotenoid-deficient maize seedling fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mrna. Eur. J. Biochem. 144: McFeeters, R.F., Chichester, C.O. and Whitaker, J.R Purification and properties of chlorophyllase from Ailanthus altissima (Tree-of-Heaven). Plant Physiol. 47: Milton, N.M., B.A. Eiswerth, and C.M. Ager Effect of phosphorus deficiency on spectral reflectance and morphology of soybean plants. Remote Sens. Environ. 36: Milton, N.M., C.M. Ager, B.A. Eiswerth, and M.S. Power Arsenic- and selenium-induced changes in spectral reflectance and morphology of soybean plants. Remote Sens. Environ. 3: Oelmullar, R., and H. Mohr Carotenoid composition in milo (Sorghum vulgare) shoots as affected by phytochrome and chlorophyll. Planta 164: Peterson, D.L., M.A. Spanner, S.W. Running, and K.B. Teuber Relationships of thematic mapper simulation data to leaf area index of temperate coniferous forests. Remote Sens. Environ. 22: Pollock, R.B., and E.T. Kanemasu Estimating leaf area index of wheat with Landsat data. Remote Sens. Environ. 8: Porra, R.J., Thompson, W.A. and Kriedelman, P.E Determination of accurate extraction and simultaneously equation for assaying chlorophyll a and b extracted with different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochem. Biophys. Acta 975: Shioi, Y., and T. Sasa Purification of solubilized chlorophyllase from Chlorella protothecoides. Methods Enzymol. 123: Thomas, J.R., and H.W. Gausman Leaf reflectance vs. leaf chlorophyll and carotenoid concentrations for eight crops. Agron. J. 69: Yang, C.M., K.W. Chang, M.H. Yin, and H.M. Huang Methods for the determination of the chlorophylls and their derivatives. Taiwania 43:

15 Chl content (µg g -1 DW.) A 2 DMF 7 DMF 5 4 B Chl a/b Nitrogen (g m -2 ) 1 Tifway 419 (A) (B) a/b DMF days mowing frequency Fig. 1. Effects of nitrogen application rate and mowing frequency on (A) Chl content and (B) Chl a/b ratio in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

16 Total porphyrin content Mole percent of Pchlide (%) Mole percent of MGPP (%) Mole percent of PPIX (%) (nmole g -1 DW.) A 2 DMF 7 DMF B C D Nitrogen (g m -2 ) 2 Tifway 419 (A) (B) PPIX (C) MGPP (D) Pchlide DMF days mowing frequency Fig. 2. Effects of nitrogen application rate and mowing frequency on (A) total porphyrin content, and mole percent of (B) PPIX, (C) MGPP and (D) Pchlide in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

17 Chlide a/b Chlide a+b (mm g -1 DW.) A B 2 DMF 7 DMF Nitrogen (g m -2 ) 3 Tifway 419 (A) Chlide a+b (B) Chlide a/b DMF days mowing frequency Fig. 3. Effects of nitrogen application rate and mowing frequency on (A) Chlide a+b content and (B) Chlide a/b ratio in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

18 Phe a+b (µg g -1 DW.) A 2 DMF 7 DMF B Phe a/b Nitrogen (g m -2 ) 4 Tifway 419 (A) Phe a+b (B) Phe a/b DMF days mowing frequency Fig. 4. Effects of nitrogen application rate and mowing frequency on (A) Phe a+b content and (B) Phe a/b ratio in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

19 Phytylated pigments A 2 DMF 7 DMF Dephytylated pigments B Nitrogen (g m -2 ) 5 Tifway 419 (A) (B) DMF days mowing frequency Fig. 5. Effects of nitrogen application rate and mowing frequency on (A) Phytylated + Dephytylated pigments content and (B) Phytylated/Dephytylated pigments ratio in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

20 Car/Chl Car (µg g -1 DW.) A 2 DMF 7 DMF B Nitrogen (g m -2 ) 6 Tifway 419 (A) (B) / DMF days mowing frequency Fig. 6. Effects of nitrogen application rate and mowing frequency on (A) Car content and (B) Car/Chl ratio in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

21 MP Car (µg g -1 dry LP Car (µg g -1 DW.) A 2 DMF 7 DMF B Nitrogen (g m -2 ) 7 Tif-way 419 (A) LP Car (B) MP Car DMF days mowing frequency Fig. 7. Effects of nitrogen application rate and mowing frequency on (A) LP Car and (B) MP Car content in the leaves of bermudagrass Tifway 419. DMF, days mowing frequency. two days mowing frequency; seven days mowing frequency.

22 5 4 A Reflectance (%) g m g m -2 5 g m Wavelength (nm) 5 4 B Reflectance (%) g m g m -2 5 g m Wavelength (nm) 8 Tifway 419 (A) (B) Fig. 8. Effects of nitrogen application rate and mowing frequency on canopy reflectance spectra of bermudagrass Tifway 419. (A) two days mowing frequency; (B) seven days mowing frequency.

23 The first order derivative of reflectance A g m g m -2 5 g m Wavelength (nm) The first order derivative of reflectance B g m g m -2 5 g m Wavelength (nm) 9 Tifway 419 (A) (B) Fig. 9. Effects of nitrogen application rate and mowing frequency on the first order derivative of canopy reflectance spectra of bermudagrass Tifway 419. (A) two days mowing frequency; (B) seven days mowing frequency.

24 A. NDVI 68 Chl a Chl b Car R 2 =.73 R 2 =.76 2 R 2 =.66 Pigment content (µg g -1 dry wt.) B. NDVI 75 Chl a R 2 =.7 Chl b Car R 2 =.72 R 2 = C. NDVI broad Chl a R 2 =.72 Chl b Car R 2 =.75 2 R 2 = NDVI 1 Tifway 419 (A) NDVI 68 (B) NDVI 75 (A) NDVI broad Chl a ( ), Chl b ( ), and Car ( ) Fig. 1. The (A) NDVI 68, (B) NDVI 75, and (C) NDVI broad versus Chl a ( ), Chl b ( ), and Car ( ) contents in bermudagrass Tifway 419.

25 1. Tifway 419 NDVI 68 NDVI 75 NDVI broad Table 1. The grey relational value and order of NDVI 68, NDVI 75, NDVI broad, and pigment contents in the leaves of bermudagrass Tifway 419. Pigment NDVI 68 NDVI 75 NDVI broad PPIX.932 (7) *.942 (7).917 (7) MGPP.8853 (11).8862 (11).8838 (1) Pchlide.6592 (14).6597 (14).6575 (14) Chl a.9222 (2).9255 (4).9189 (2) Chl b.886 (1).889 (1).8832 (11) Chlide a.825 (13).8215 (13).8191 (13) Chlide b.8341 (12).8349 (12).8328 (12) Phe a.913 (6).9157 (6).998 (5) Phe b.9133 (5).917 (5).983 (6) Phytylated pigments.9165 (3).9261 (3).9115 (3) Dephytylated pigments.8993 (8).912 (8).8977 (8) Car.9326 (1).9389 (1).9292 (1) LP Car.9159 (4).928 (2).9111 (4) MP Car.8964 (9).8975 (9).8949 (9)

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