Abstract
Male reproductive development of rice (Oryza sativa L.) is very sensitive to drought. A brief, transitory episode of water stress during meiosis in pollen mother cells of rice grown under controlled environmental conditions induced pollen sterility. Anthers containing sterile pollen were smaller, thinner, and often deformed compared to normal anthers of well-watered plants. Only about 20% of the fully developed florets in stressed plants produced grains, compared to 90% in well-watered controls. Water stress treatments after meiosis were progressively less damaging. Levels of starch and sugars and activities of key enzymes involved in sucrose cleavage and starch synthesis were analyzed in anthers collected at various developmental stages from plants briefly stressed during meiosis and then re-watered. Normal starch accumulation during pollen development was strongly inhibited in stress-affected anthers. During the period of stress, both reducing and non-reducing sugars accumulated in anthers. After the relief of stress, reducing sugar levels fell somewhat below those in controls, but levels of non-reducing sugars remained higher than in controls. Activities of acid invertase and soluble starch synthase in stressed anthers were lower than in controls at comparable stages throughout development, during as well as after stress. Stress had no immediate effect on ADP-glucose pyrophosphorylase activity, but had an inhibitory aftereffect throughout post-stress development. Sucrose synthase activity, which was, relatively speaking, much lower than acid invertase activity, was only slightly suppressed by stress. The results show that it is unlikely that pollen sterility, or the attendant inhibition of starch accumulation, in water-stressed rice plants are caused by carbohydrate starvation per se. Instead, an impairment of enzymes of sugar metabolism and starch synthesis may be among the potential causes of this failure.
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References
Banga SS, Labana KS, Banga SK (1984) Male sterility in Indian mustard (Brassica juncea (L.) Coss.) — a biochemical characterization. Theor Appl Genet 67: 515–519
Bhadula SK, Sawhney VK (1989) Amylolytic activity and carbohydrate levels during the stamen ontogeny of a male fertile and a ‘gibberellin-sensitive’ male sterile mutant of tomato (Lycopersicon esculentum). J Exp Bot 40: 789–794
Bingham J. (1966) Varietal response in wheat to water supply in the field and male sterility caused by a period of drought in a glasshouse experiment. Ann Appl Biol 57: 365–377
Boyer JS, McPherson HG (1975) Physiology of water deficits in cereal crops. Adv Agron 27: 1–23
Brooking IR (1976) Male sterility inSorghum bicolor (L.) Moench induced by low night temperature. I. Timing of the stage of sensitivity. Aust J Plant Physiol 3: 589–596
Bryce WH, Nelson OE (1979) Starch-synthesizing enzymes in the endosperm and pollen of maize. Plant Physiol 63: 312–317
Carlson M, Osmond BC, Botstein D (1981) Mutants of yeast defective in sucrose utilization. Genetics 98: 25–40
Chourey PS, Nelson OE (1979) Interallelic complementation at the sh locus in maize at the enzyme level. Genetics 91: 317–325
Clément C, Chavant L, Burrus M, Audran JC (1994) Anther starch variations inLilium during pollen development. Sex Plant Reprod 7: 347–356
Cruz RT, O'Toole JC (1984) Dryland rice response to an irrigation gradient at flowering stage. Agron J 76: 178–187
Dembinska O, Lalonde S, Saini HS (1992) Evidence against the regulation of grain set by spikelet abscisic acid levels in waterstressed wheat. Plant Physiol 100: 1599–1602
Ekanayake IJ, Steponkus PL, De Datta SK (1990) Sensitivity of pollen to water deficits at anthesis in upland rice. Crop Sci 30: 310–315
Fischer RA (1973) The effect of water stress at various stages of development on yield processes in wheat. In: Slatyer RO (ed) Plant responses to climatic factors, Proc. Uppsala Symposium. UNESCO, Paris, pp 233–241
Graham RD (1975) Male sterility in wheat plants deficient in copper. Nature 254: 514–515
Hanson AD, Hitz WD (1982) Metabolic responses of mesophytes to plant water deficits. Annu Rev Plant Physiol 33: 163–203
Hawker JS, Jenner CF, Niemietz CM (1991) Sugar metabolism and compartmentation. Aust J Plant Physiol 18: 227–237
Ito N (1978) Male sterility caused by cooling treatment at the young microspore stage in rice plants. XVI. Changes in carbohydrates, nitrogenous and phosphorous compounds in rice anthers after cooling treatment. Jpn J Crop Sci 17: 318–323
Jenner CF (1982) Storage of starch. In: Loewus FA, Tanner W (eds) Plant carbohydrates. I. Intracellular carbohydrates. (Encyclopedia of plant physiology, new series, vol 13A) Springer, Berlin Heidelberg New York, pp 700–747
Jenner CF, Siwek K, Hawker JS (1993) The synthesis of [14C]starch from [14C]sucrose in isolated wheat grains is dependent upon the activity of soluble starch synthase. Aust J Plant Physiol 20: 329–335
Joppa LR, McNeal FH, Welsh JR (1966) Pollen and anther development in cytoplasmic male sterile wheat (Triticum aestivum L.) Crop Sci 6: 296–297
Keeling PL, Bacon PJ, Holt DC (1993) Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191: 342–348
Miki-Hirosige H, Nakamura S (1983) Growth and differentiation of amyloplasts during male gamete developmentin Lilium longiflorum. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier Biomedical, New York, pp 141–147
Miller ME, Chourey PS (1992) The maize invertase-deficientminiature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4: 297–305
Morgan JM (1980a) Possible role of abscisic acid in reducing seed set in water-stressed wheat plants. Nature 285: 655–657
Morgan JM (1980b) Osmotic adjustment in the spikelets and leaves of wheat. J Exp Bot 31: 655–665
Nakamura N, Sado M, Arai Y (1980) Sucrose metabolism during the growth ofCamellia japonica pollen. Phytochemistry 19: 205–209
Nakamura Y, Yuki K, Park S-Y, Ohya T (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30: 833–839
Nakamura N, Suzuki Y, Suzuki H (1992) Pyrophosphate-dependent phosphofructokinase from pollen: properties and possible roles in sugar metabolism. Physiol Plant 86: 616–622
Namuco OS, O'Toole JC (1986) Reproductive stage water stress and sterility. I. Effect of stress during meiosis. Crop Sci 26: 317–321
Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153: 375–380
O'Toole JC, Moya TB (1981) Water deficits and yield in upland rice. Field Crops Res 4: 247–259
O'Toole JC, Namuco OS (1983) Role of panicle exsertion in water stress induced sterility. Crop Sci 23: 1093–1097
Pacini E, Franchi GG (1988) Amylogenesis and amylolysis during pollen grain development. In: Cresti M, Gori P, Pacini E (eds) Sexual reproduction in higher plants. Springer, Berlin Heidelberg New York, pp 181–186
Pheloung P, Barlow EWR (1981) Respiration and carbohydrate accumulation in the water-stressed wheat apex. J Exp Bot 32: 921–931
Plaxton WC, Preiss J (1987) Purification and properties of nonproteolytic degraded ADP-glucose pyrophosphorylase from maize endosperm. Plant Physiol 83: 105–112
Preiss J (1988) Biosynthesis of starch and its regulation. In: Preiss J (ed) The biochemistry of plants, vol 14. Academic Press, San Diego, Calif, pp 181–254
Saini HS, Aspinall D (1981) Effect of water deficit on sporogenesis in wheat (Triticum aestivum L.) Ann Bot 48: 623–633
Saini HS, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Ann Bot 49: 835–846
Saini HS, Sedgley MS, Aspinall D (1984) Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Aust J Plant Physiol 11: 243–253
Salter PJ, Goode JE (1967) Crop responses to water at different stages of growth. Commonw. Agric. Bur., Farnham Royal, England, pp 15–48
Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimation of pollen development stage and the most stage to coolness. Proc Crop Sci Soc Jpn 39: 468–473
Sato K (1954) Relationship between rice crop and water. Jpn J Breed 4: 264–289
Skazkin FD, Zavadskaya IG (1957) On the influence of soil moisture deficiency and nitrogen nutrition on microsporogenesis in barley. Dokl Akad Nauk SSSR 117: 240–242
Skazkin FD, Lukomskaya KA (1962) Effect of soil water deficiency on formation of female gametophyte. Dokl Akad Nauk SSSR 147: 1173–1174
Smith AM, Denyer K, Martin CR (1995) What controls the amount and structure of starch in storage organs? Plant Physiol 107: 673–677
Stanley RG, Linskens HF (1974) Pollen — biology, biochemistry, management. Springer, Berlin Heidelberg New York, pp 307
Stitt M (1994) Manipulation of carbohydrate partitioning. Curr Opin Biotechnol 5: 137–143
Tsai CY, Salamini F, Nelson OE (1970) Enzymes of carbohydrate metabolism in the developing endosperm of maize. Plant Physiol 46: 299–306
Wells SA, Dubetz S (1966) Reaction of barley varieties to soil water stress. Can J Plant Sci 46: 507–512
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57: 508–514
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Sheoran, I.S., Saini, H.S. Drought-induced male sterility in rice: Changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sexual Plant Reprod 9, 161–169 (1996). https://doi.org/10.1007/BF02221396
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DOI: https://doi.org/10.1007/BF02221396