J. E. Irvine USDA Houma, Louisiana
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1 Weed Control, Plant Physiology and Biochemistry PHOTOSYNTHETIC RATE IN SUGARCANE: EFFECT OF VIRUS DISEASES, GENETIC DISORDERS, AND FREEZING J. E. Irvine USDA Houma, Louisiana ABSTRACT Photosynthesis per unit area and chlorophyll content were reduced by sugarcane. mosaic virus, variegation, freezing, and "red-freckle." Photosynthesis per unit of chlorophyll was increased by sugarcane mosaic virus, 'variegation and freezing, and was reduced by "red-freckle." Chlorotic streak disease and ratoon stunting disease had no significant effect on the rate of photosynthesis. IN'IRODUCTION Studies of the environmental factors affecting photosynthesis in sugarcane include light (7,10,15), CO 2 concentration (7,18), time of day (10), injury (7), fertility (7), air temperature (7,18), and air flow rates (14). Internal factors associated with photosynthesis in sugarcane include leaf age and rank (7,18), variety (11), respiration (12), moisture content (7), stalk sucrose content (18), stomatal behavior (11,14), and virus infection (13). Physiological, pathological, and genetic disorders (10) cause anomalies which could indicate photosynthetic impairment and reduction in productivity. Mineral deficiencies cause chlorosis and reduction in photosynthetic rate (7). Virus infections which cause mosaic patterns may reduce cholorophyll content (11,17), deform chloroplasts (3,6), and impair biochemical functions associated with photosynthesis (8,9,19). Mutations or chimeras which cause color variants or variegated forms have been associated with changes in photosynthetic activity (15). Infection of sugarcane varieties with strains of sugarcan<:: mosaic virus (SCMV) caused a reduction in chlorophyll content and in photosynthetic activity per unit area (13). However, the reduction in the rate of photosynthesis was not paralleled by symptom severity, and the rate of photosynthesis on a unit chlorophyll basis was actually increased. Chlorotic streak, ascribed to a virus, causes a reduction in :total green leaf area and a localized deformation and destruction of chloroplasts in sugarcane leaves with symptoms (3). The virus disease, ratoon stunting disease, which exhibits no leaf symptoms, is known to reduce yields under field conditions. Freezing frequently may cause tissue death and destruction of chlorophyll over large areas of sugarcane leaves. streaks may remain in the leaves, and leaebases may remain green even though terminal buds have been killed. The visual result ina field of cane is that of a green band between the canopy and stalks, an area that might retain significant photosynthetic activity. 1131
2 1132 WEED CONTROL, ETC. The purpose of this study was to investigate several disorders that might affect the rate of photosynthesis of sugarcane leaves. and lower productivity. MATERIALS AND METHODS The rate of photosynthesis was measured on leaves of intact plants by sealing a part of the lamina between two halves of an acrylic plastic leaf chamber (56 X lox 1 em). The chamber was aerated with moist (82% RH) air with a flow rate of 5 l/min. Care was taken to insure that entering and exiting airstreams flowed at the same rate. The flow rate chosen gives intermediate rates of photosynthesis (14). The amount of CO 2 removed by the leaf was. determined with an infra-red analyzer (Beckman M2l5) by sampling both air leaving the chamber and air by-passing it. Air to be sampled entered the analyzer cell at a slight positive pressure. The analyzer cell temperature was maintained at 22 C, and in the calculations of mg CO 2 /l, temperatures were corrected according to the perfect-gas equation... Light was supplied by l500e Quartz-iodide tubes screened by water and by cheesecloth filters. The leaf blade, in its enclosing chamber, was exposed to 3 X 10 5 erg cm" S-l for 30 min and then to 8 X 10 5 erg cm- 2 S-l for 20 min before a measurement was taken. The latter intensity approached that of full sun at 660 nm (14). Since only trace amounts of CO 2 escape from sugarcane leaves at high light intensities (12), no corrections are made for respiration; and the results are expressed as true.photosynthesisin ing CO 2 absorbedjdm-j'hr. Immediately after the rate of photosynthesis at high light intensity was determined, the chamber was opened and leaf porosity was measured with an Alvimiporometer. The area, width, and thickness of the leaf were measured and the weight per unit area determined. Plant height was measured from soil level to the dewlap of the youngest fully expanded leaf, and the number of leaves between ground level and this leaf was counted. Disease symptoms were recorded when present. The area of the leaf which had been enclosed in the leaf chamber was extracted with acetone (spectral grade) for chlorophyll estimations (5). In 1970, the effects of 5 sugarcane mosaic virus (SCMV) strains on photosynthesis were studied. Single bud cuttings of sugarcane variety CP were incubated, planted in pots, and grown in a greenhouse equipped with 30-mesh screen. Three weeks. after potting, plants were inoculated with SCMV strains A, B, D, H, or 1. Healthy plants, 3 months old, were compared to plants infected with the 5 SCMV strains. Determinations of the rate of photosynthesis were made on the youngest fully expanded leaf, the 9th, 10th, or 11th leaf to be produced. Five plants per treatment were used. Data were analyzed by an analysis of variance for a randomized block design followed by mean separation with Duncan's multiple range test. The effects of variegation on photosynthesis were studied in a greenyellow variegated form of PO] 234 and a green-white variegated form of CP The green area of variegated leaves was determined by tracing the outline of the total leaf area on paper of a known weight per unit area and determining total area. The leaf was weighed and the green tissue excised. The green tissue was weighed and the green leaf area determined by proportion. Photosynthetic rates, chlorophyll content and chlorophyll-free area were deter-
3 J. E. IRVINE 1133 mined on leaves of differing degrees of variegation. The variegated forms of both varieties appear to be periclinal chimeras (16). The plant of POJ 234 appears to be a green on white chimera and that of CP appears to bea white on green chimera... Plants of L were used to determine the effects of freeze damage on photosynthetic activity. Plants grown in 6-in. pots for 6 months were placed in a walk-in freezer at 23 F. The plants remained in the freezer about 4 hr until water-soaked streaks appeared on the leaves. The freeze-treated plants were replaced in the greenhouse for 2 weeks while the freeze symptoms became stabilized. Freeze-damaged leaves on 5 plants were measured for photosynthetic activity and chlorophyll content and the data were compared with that from unfrozen plants of the same variety... Plants with the red-freckle syndrome were obtained from single bud cuttings of CP The plants were grown as described for the study of mosaic strains. Healthy plants were compared to those showing the typical reddening of the older leaves. Plants of both categories were grown in 15-cm clay pots for 4 months before studies were initiated on rates of photosynthesis. Leaves on the plants were assigned numbers based on their position on the plant, with the youngest fully exposed leaf having exposed dewlap designated as leaf I; older leaves were designated 2, 3, etc.: younger leaves were designated 0, -1, etc. In this experiment only leaves 1-3 were sampled on each plant. Photosynthetic rate, chlorophyll content, leaf porosity, symptom severity and plant height were determined. In a second experiment, cut leaves were harvested from a replicated field experiment. Cut leaves have lower photosynthetic rates than attached leaves (14,18). In this study leaves designated -I, 0, I, 2, and 3 were sampled on each plant. The cut ends of healthy and abnormal leaves were immediately placed in water and transported to the laboratory. Rates of photosynthesis were obtained as described, and observations were made on symptom severity and chlorophyll content. Plants with chlorotic streak disease (CSD) were propagated from cuttings of NCo 310 taken from stalks showing the leaf symptoms of the disease. These plants were grown in an unscreened greenhouse during the summer of Healthy and diseased plants were. maintained in the same area but not on the same benches. Comparisons of the rate of photosynthesis, chlorophyll content and growth were made between healthy plants and plants with and without leaf symptoms. Plants with ratoon stunting disease (RSD) were propagated from cuttingsof CP taken from stalks that showed the mature stalk symptoms. Diseased : plants were randomized on the same bench with healthy plants obtained from cuttings from symptom-free stalks descended from direct hot-watertreated plants. Comparisons of photosynthesis rates, chlorophyll content, height and porosity were made on the youngest hilly expanded leaves (leaf 1). Each plant was examined for the internal juvenile RSD symptom after other measurements were complete. RESULTS Plants of CP infected with 1 of 5 strains of mosaic produced symptoms typical for the strain on this differential host (4). Plants with strains A,
4 1134 WEED CONTROL, ETC. B, D, or H could be separated on the basis of symptoms; strains H and I could not be so separated. Non-inoculated plants remained free of symptoms. Chlorophyll content per unit area paralleled the symptom severity ratings (Table 1). Table 1. The effects of sugarcane mosaic virus strains on symptom expression, chlorophyll content, photosynthesis and height of CP Photosynthetic rate Chlorophyll per unit per unit SCMV Visible content area chlorophyll Height strain symptoms (mg s dm-a) (mg' dm-2, h-1) (mg' mg 'h- 1 ) (em) Healthy None' 6.22 a a 4.45 b 67.6 a Strain A Mild 5.14 ab a 5.51 ab 48;0 b Strain B Severe 4.15 ab b 5.64 ab,40.4 b Strain D Severe 3.61 b b 6.02 a 37:6' b Strain H Mild 5.98 ab a 4.57 b 40.2 b Strain I Mild 5.43 ab b 4.54 b 40.0 b Means in the same column sharing the same letter are not different at the 5% level of probability. Plants with no symptoms and plants with SCMV strains A and H had the highest rates of photosynthesis per unit,;:trea and the lowest rates of photosynthesis per unit of chlorophyll. Plants infected with SCMV strains B, D, and I were significantly lower in photosynthetic activity per unit area. Onlyplants infected with SCMV strain D showed a significantly higher photosynthetic rate on a unit chlorophyll basis. Plant height measured at the time of photosynthesis determinations was significantly lower in plants infected with all strains than in healthy plants. No significant differences in height occurred between plants infected with the different strains of SCMV. No significant differences in leaf porosity were detected. Plants of CP and PO] 234 with variegated leaves showed a reduction in chlorophyll content and in photosynthesis per unit area in plants with the amount of green leaf area reduced by variegation. A completely white leaf of CP contained no extractable chlorophyll and exhibited no photosynthetic activity. Leaf chamber air flow rates ranging from l/min produced no detectable decrease in CO 2 content of the air leaving the chamber. With flow rates of 2 ljmin or less a slight increase in CO 2 content was noted, indicating respiratory release of CO 2 in the light by the albino leaf. Leaves of PO] 234 with green-yellow variegation showed a reduction of chlorophyll and photosynthesis per unit area in leaves with less green leaf tissue (Table 2). Conversely, photosynthetic activity per unit of chlorophyll tended to increase as the amount of green leaf area and chlorophyll content decreased. The freezing of leaves of the variety L caused a reduction in the total area of chlorophyll-bearing tissue. The terminal portions of the leaves were completely brown 2 weeks after freezing, with streaks of green tissue in the center coalescing towards the base of the leaf. The chlorophyll content was reduced from 5.81 to 1.77 mg'dm- 2 and the rate of photosynthesis per unit area was reduced from to mg'dm- 2'h-1 The rate of photosynthesis per unit of chlorophyll was increased from 5.02 to 8.55 mg'mg'h- 1
5 F'-"'~-"'" ) c { -----~----'---.~"""~~--- J.,E. IRVINE 1135 Table 2. leaf area, chlorophyll content and photosynthetic acitvity in variegated sugar" cane leaves. Mg C02 absorbed leaf Chlorophyll area content per unit per mg (%) (mg'dm- 2 ) area chlorophyll 0" l.(}l , , ll " Values with an asterisk are from CP ; other values are those from PO] 234. Plants of CP with and without the red-freckle symptoms differed in photosynthetic activity and chlorophyll content (Table 3). No differences in appearance, in chlorophyll content or in photosynthetic activity were detectable in leaves 1 and 2 of normal and abnormal greenhouse plants. Leaf 3 showed distinctive red stippling or freckling beginning near the mid-rib and progressing toward the margin. Leaf 3 of plants with these symptoms was significantly lower than healthy plants in photosynthetic activity. The rate of photosynthesis was reduced both on an area and a unit chlorophyll basis. Field-grown plants with red-freckle symptoms were severely stunted in contrast to greenhouse plants. Only the youngest leaves sampled (lea -r- 1) of field plants lacked reddening and had nearly normal photosynthetic rates. Older,leaves showed a marked increase in reddening, a marked decrease in chlorophyll content and a decrease in photosynthesis, both per unit area and per unit of chlorophyll. Plants of the variety NCo 310 infectedwith chlorotic streak disease were not significantly different from healthy plants in photosynthetic activity or in plant height. Leaves with CSD symptoms, from 10 plants, yielded an average photosynthetic rate of mg' drrr-' h-l, while leaves from 10 healthy plants yielded an average rate of mg' dm~2 ' h-l, not a significant difference. There was a slight reduction in chlorophyll content, and the area of the leaf blade with chlorophyll was 3% less in leaves with symptorns. Plants of. the variety CP infected with RSDwere not different from healthy plants in rate of photosynthesis, chlorophyll content, porosity, or plant height. The photosynthetic rate of leaf} of 10 RSD infected plants averaged mg'dm- 2'h-1and the rate of leaf I'df 10 healthy plants mg'dm- 2'h-1 The juvenile symptoms of RSD were present in all diseased plants and were absent in all healthy controls. DISCUSSION While the disorders investigated had caused reductions in productivity
6 1136 WEED CONTROL, ETC. Table 3: The effect of red-freckle syndrome on photosynthesis in CP Leaf numberi Treatment -1 o Healthy Red-freckle Healthy Red-freckle Healthy Red-freckle Young greenhouse plants Color Chlorophyll content Photosynthesis per unit area (attached leaves) (mg > dm-e) (mg' dm-a- h-1) a a Photosynthesis per unit of chlorophyll 5.73 a 5.66 a 5.30 a 5.59 a a a (mg s mg e h-ij Healthy a 4.72 a Red-freckle a 4.50 a Mature field plants Color (Cut leaves) Red 5.44 a 3.03 b a b 4.92 a 4.00 b Healthy Red-freckle Red Red Reel Reel Chlorophyll content (mg' dm-2) Healthy Red-freckle Photosynthesis per unit area (mge dm-2 h-x). Healthy Red-freckle Photosynthesis per unit of chlorophyll (mg' mg' h-1) Healthy Red-freckle Means of the same parameter sharing the same letter are not significantly different at the 5% level of probability. either in the field or greenhouse, only leaves with symptoms of SCMV, variegation, freezing, or red-freckle showed reductions in rate of photosynthesis. The plants infected with chlorotic streak and RSD had normal rates of photosynthesis. The data in Table I are in general agreement with those published on the reactions of CP to strains of sugarcane mosaic (2). There are differences in the response of CP to the different strains, including different symptoms, different rates of photosynthesis in plants infected with the same strain, and different growth responses. However, strain D produced the greatest reduction of chlorophyll and photosynthetic activity in both varieties. In both vari-
7 J. E. IRVINE 1137 eties, syinptom severity was not paralleled by photosynthetic activrty. Plants of CP infected by strain A had severe local symptoms but no change in photosynthesis per unit area (13). Plants of CP infected by strain I had mild. symptoms but the rate of photosynthesis per unit area was significantly reduced. Infection with SCMV tended to increase the rate of photosynthesis per unit of chlorophyll in both varieties (strains A, B, D and I in CP , strain D in CP ).. Reduction of chlorophyll content and photosynthetic activity also occurred in healthy leaves in which the green leaf area was reduced by variegation. The reduction in green leaf area and chlorophyll content was accompanied by decreases in photosynthesis per unit area and increases in photosynthesis per unit of chlorophyll. Normal green leaves contain more chlorophyll than is required.for maximum photosynthesis (15); thus, when photosynthesis is expressed on a unit chlorophyll basis the rates appear low. If this chlorophyll surplus is reduced without adversely affecting chloroplast functions, the rate of photosynthesis per unit of chlorophyll increases and the chlorophyll unit appears more efficient, even though the photosynthetic rate per unit area may be less. Lower rates of photosynthesis per unit area may be due to less green leaf area or to reduced dark reaction rates or reduced translocation. When a reduced rate of photosynthesis per unit area is accompanied by a similar reduction per unit of chlorophyll, an impariment of chlorophyll function is suggested. These reductions occurred in leaves showing SCMV, variegation, freezing, and red-freckle symptoms. As in all leaves with these symptoms, the reduction in photosynthesis per unit area was accompanied by a reduction in chlorophyll per unit area. Unlike leaves with other symptoms, leaves with red-freckle also showed a reduction in photosynthesis per unit of chlorophyll. This suggests an impairment of chloroplast function in addition to chlorophyll reduction in redfreckle. REFERENCES 1. Abbott, E. V Influence of certain environmental conditions on chlorotic streak of sugarcane. Phytopath,37: , C. G. Hughes, and J. P. Martin Chlorotic streak, p In Jo P. Martin, E. V. Abott, and C. G. Hughes [Ed]. Sugarcane Diseases of the World. Vol. 1. Elsevier, Amsterdam. 3., and j. E. Sass Pathological histology of sugarcane affected with chlorotic streak. Jour. Agr. Res., 70:lWl , and R. L. Tippett Strains of sugarcane mosaic virus. USDA Tech. Bull Arnon, D. I. )949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol., 24:1-15. / 6. Esau, K Viruses in Plant Hosts. Univ. Wise, Press, Madison. 7. Hartt, C. E., and G. D. Burr. ISSCT, 12: Factors affecting photosynthesis in sugarcane..... Proc. 8. Hopkins, D. L., and R. E. Hampton Effects of tobacco etch virus upon the light reactions of photosynthesis in tobacco leaf. tissue. Phytopath., 59: , and Effects of tobacco etch virus infection upon the dark reactions of photosynthesis in tobacco leaf tissue. Phytopath., 59: Hughes, C. G Genetical effects.p In C. G. Hughes, E. V. Abbott and C. A. Wismer [Ed]. Sugarcane Diseases of the World. Vol. 2. Elsevier, Amsterdam.
8 1138 WEED CONTROL, ETC. 11. Irvine, J. E Photosynthesis of sugarcane varieties under field conditions. Crop Sci., 7: Evidence for photorespiration in tropical grasses. PhysioI. Plant., 23: Photosynthesis of sugarcane varieties infected with strains of sugarcane mosaic virus. PhysioI. Plant., 21: ,71. Photosynthesis and stomatal behavior in sugarcane leaves as affected by light intensity and low air flow rates. PhysioI. Plant. In press. 15. Rabinowitch, E. J Photosynthesis and Related Processes. Interscience, New York. 16. Thielke, C. H Principles of chimeral variegation in grasses. Sugarcane Pathologists Newsletter, 5: Tu, J. C., R. E. Ford, 'and C. J. Krass Comparisons of chloroplasts and photosynthetic rates of plants infected and not infected by maize dwarf mosaic virus.. Phytopath., 58: Waldron, J. C., K. T. Glasziou, and T.,A. Bull The physiology of sugarcane IX. Factors affecting photosynthesis and sugar storage. Aust. J. BioI. Sci., 20: Zaitlin, M., and A. T. Jagendorf Photosynthetic phosphorylation and FIill reaction' activities of chloroplasts isolated from plants infected with tobacco mosaic virus. Virology, la:
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