Cotyledon Photosynthesis During Seedling Growth of Cotton, Gossypium hirsutum L.Author(s): H. C. Lane and J. D. HeskethSource: American Journal of Botany, Vol. 64, No. 6 (Jul., 1977), pp. 786-790Published by: Botanical Society of AmericaStable URL: http://www.jstor.org/stable/2441731 .

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Amer. J. Bot. 64(6): 786-790. 1977.

COTYLEDON PHOTOSYNTHESIS DURING SEEDLING GROWTH OF COTTON, GOSSYPIUM HIRSUTUM L.'

H. C. LANE AND J. D. HESKETH Cotton Production Research, Agr. Res. Serv., USDA, Mississippi State, MS 39762

A B S T R A C T Respiration and net photosynthetic 02 production by cotton cotyledons were determined

from an early age through the senescent stage. Various treatments were applied to cotyledons to assess the importance of current photosynthesis as compared to translocation of reserves to seedling development. Rates of respiration and net photosynthesis per cm2 were high on 1- day-old cotyledons, but the rates decreased sharply with rapid expansion to reach a fairly stable rate. Respiration per cotyledon decreased linearly with age until the onset of senescence, then exhibited a distinct climacteric rise followed by a sharp decrease. Net photosynthesis per coty- ledon increased until expansion was completed and then decreased linearly and steeply with age. Excision of cotyledons, inhibition of photosynthesis either chemically or by covering, and removal of the terminal bud indicated that current photosynthesis is a potent force behind early epicotyl growth.

COTTON cotyledons expand to green, persistent structures soon after emergence. Richardson (1967) noted that the photosynthetic compensa- tion point of cotton seedlings was reached 24 h after emergence, and that a stable rate was attained 200 h after emergence. El-Sharkawy, Hesketh and Muramoto (1965) measured rates of cotton cotyledon photosynthesis of various genotypes of unspecified ages and observed rates ranging from 19 to 49 mg C02/dm2/h.

To our knowledge, there are no definitive re- ports on the respiratory and photosynthetic activi- ties of cotton cotyledons from an early to senescent stage. We measured respiration and net photo- synthetic 02 evolution over a period from 1 to 42 days of age. To assess further the role of cotyledon photosynthesis in sustaining the seedling and en- hancing seedling growth, we compared the effects of a) removal of the cotyledons, b) treatment with a specific photosynthetic inhibitor, and c) covering cotyledons with aluminum foil. Finally, we compared the gain in cotyledon weight of con- trol seedlings to seedlings with the terminal bud removed.

MATERIALS AND METHODS-Seeds (cv. Stone- ville 1 8524-glandless) were planted in 15-liter pots containing a 1:1:1 mixture of peat moss, vermiculite, and perlite. The seedlings were grown under natural light, watered as needed, and

1:Received for publication 11 October 1976; revision accepted 3 March 1977.

Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that may also be suitable.

given 1 liter of standard Hoagland's solution twice weekly. The seedlings were said to be 1 day old 24 h after straightening of the hypocotyl hook. One series of measurements of respiration and net photosynthesis was started in March, another in May. All measurements were pooled when an analysis of variance showed no significant varia- tion due to series. All data shown are means of eight observations.

Oxygen uptake and evolution were measured with a YSI model 5331 02 electrode and a YSI model 53 biological O2 monitor. A complete de- scription of the method is provided elsewhere (Lane, 1977). A 1 cm2 section of cotyledon was immersed in air-saturated 0.05 M phosphate buffer pH 5.8 containing 5 mm NaHCO3. After an initial setting of the probe to 100% saturation on air-saturated buffer, 02 uptake was measured in the dark to 70% saturation. Then, in light, 02 evolution was measured back to 100% saturation. The results are reported as 1A 02/h.

Light was furnished by a 500 w projector lamp at 110 V after filtering by a 6 mm thick heat ab- sorbing glass and 10 cm of water (Withrow, 1957). The light intensity at the surface of the tempera- ture control jacket was 1.1 cal/cm2/min. The light intensity on the cotyledon section was slightly less because of an additional cm of water and two thin sections of glass. All measurements were made at 28 C.

To measure the effects of excision of cotyledons, inhibition of photosynthesis either by chemical inhibition or exclusion of light, lots of 4-day-old seedlings were paired. One of each pair had a) cotyledons removed, b) cotyledons dipped for 15 sec in a solution of 5 x 10-4M 3-(3,4-dichloro- phenyl)-1,1-dimethylurea (DCMU) or c) cotyle-

786

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July, 1977] LANE AND HESKETH-COTYLEDON PHOTOSYNTHESIS OF COTTON 787

27 0

24 0 0

21 o

18

15 0

< 12 w < 9

6-

3

. . . I , I

0 7 14 21 28 35 42

AGE (days) Fig. 1. Expansion of cotyledons with age.

dons covered with foil. The dry weight of epicotyl growth was taken after a variable period of time. On another lot of paired seedlings, the terminal bud was removed on one and the gain in dry weight of cotyledons on control and treated seed- lings was taken after 11 days.

RESULTS-Cotyledon growth-Cotyledons ex- panded very rapidly during the first 7 days; then the rate of expansion progressively declined until maximum size was reached ca. 21 days after emergence (Fig. 1). The cotyledons maintained a green, glossy color through 28 days. Incipient chlorosis was evident in most 35-day-old cotyle- dons, and those available at 42 days either showed increased signs of senescence or were completely void of green color (yellow) and almost ready to abscise.

Dark respiration-The rate of respiration for 1-day-old cotyledons was very high and variable on a unit area basis (Fig. 2A). The rate decreased rapidly with expansion but reached a stable level at 7 days which was fairly uniform through 28 days. The rate of respiration for 35-day-old coty- ledons increased in both the March and May series over that for 28 days (Fig. 2A, 2B). The rate of

200

160 A

120\

r- 80 0

40

1600 B

._ 1200

,. 800

0 400

* p I_ . . * ........

7 14 21 28 35 42

AGE (days) Fig. 2. Respiration in ti/lh (A) on cm2 basis (S for

1-day-old was 43), and (B) per cotyledon basis.

respiration at 42 days had dropped sharply from that at 35 days and was lower than at any other age (Fig. 2A, 2B).

Net photosynthesis-Net photosynthesis per unit area decreased during the first 7 days (Fig. 3A), but that decrease was more than compen- sated by expansion (Fig. 3B). Net photosynthesis per unit area also reached a stable rate after 7 days and was maintained until expansion was com- pleted, then decreased linearly with age. Net photosynthesis per cotyledon increased with ex- pansion, but once full size was attained, the rate showed a steep linear decrease (Fig. 3B).

Effects of excision and inhibition of photosyn- thesis on epicotyl development-Survival of seed- lings in which the cotyledons were excised varied from 50 to 90% in two tests. The growth of the epicotyl of surviving seedlings was very slow. The epicotyls were harvested 11 days after excision when growth of the first true leaf began. The comparison between epicotyl growth of paired seedlings is given in Table 1.

Treatment with DCMU inhibited photosynthe- sis 100% when tested 4 days posttreatment. No

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788 AMERICAN JOURNAL OF BOTANY [Vol. 64

inhibition-of photosynthesis was measured on the 6th day posttreatment for sections from green areas of the cotyledon. About 50% of the surface of the treated cotyledons showed distinct chlorosis, and in those areas photosynthesis was inhibited 66%. Higher concentrations of DCMU were too toxic to be useful. Nonetheless, the temporary and incomplete inhibition by a 5 x 10-4M concen- tration caused a significant reduction in the growth of the epicotyls (Table 1).

Seedlings were not killed when the cotyledons were covered with foil. However, the treatment inhibited or delayed epicotyl growth to the same extent as excision of cotyledons (Table 1). There was no significant change in the dry weight of the covered cotyledons during the treatment. During the interval, there was considerable epicotyl growth on the control plants and there was an increase in the average dry weight of the cotyledons of 44 mg (Table 1).

Effect of removal of terminal bud on dry weight gain of cotyledons-The average dry weight of 12 randomly selected 4-day-old cotyledons was 26 mg. Eleven days after removal of the terminal buds, the mean dry weights of cotyledons on treated seedlings and the controls were 228 mg and 122 mg, respectively. The change in dry weight of cotyledons of the treated and control seedlings is shown in Table 1.

DISCUSSION-The cotton cotyledon, like some other epigeal cotyledons, bears stomates on both surfaces, undergoes a period of expansion, is dark green, and persistent. Its photosynthetic capability is not surprising. Comparatively, the more dis- tinguishing features of the cotton cotyledon are its considerable expansion and its long functional life span (Ampofo, Moore, and Lovell, 1976; Lovell and Moore, 1970, 1971; McAlister and Kroher, 1951; Sasoki and Kozlowski, 1968).

300

240 A

- 180 E t 120 0 O 60

4000 B

3000

- 2000 0

1000

7 14 21 28 35 42

AG E (days) Fig. 3. Photosynthetic 02 evolution (A) on cm2 basis

(S for 1-day-old was 43.6), and (B) per cotyledon basis.

The respiratory and photosynthetic activities of cotton cotyledons follow much the same pattern as that of true leaves of cotton and some other plants (Elmore, Hesketh, and Muramoto, 1967; Woolhouse, 1967). Respiration is very high just after emergence, or when one would expect that reserves are being translocated to the growing axis.

TABLE 1. Mean dry weights of epicotyls and change in mean dry weights of cotyledons following various treat- ments

Mean dry weight Change in mean Treatment Days No. of epicotyls dry weight cotyledons

of cotyledons posttreatment pairs (mg) * (mg) *

Excised 11 9 29 Control 11 9 268

DCMU dipped 6 12 60 Control 6 12 158

Covered 11 8 25 +0.7 Control 11 8 245 +44

Terminal bud removed 11 8 +176 Control 11 8 +60

* Means within treatments are all significantly different at the 1% probability level.

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July, 1977] LANE AND HESKETH-COTYLEDON PHOTOSYNTHESIS OF COTTON 789

As the cotyledon adapts to its aerial environment and changes to an assimilatory organ, respiration decreases to reach a rate that is uniform over most of its life span (Fig. 2A). Then, as in the leaves of several plants, a clear-cut climacteric rise is observed at the onset of senescence (Fig. 2B; Biale, 1975). Respiration decreases to a much lower rate as senescence advances and abscission starts.

Seedlings just emerged are dark green and have a high photosynthetic capacity which on an organ basis increases until expansion is completed. Then, also like leaves, the rate drops with age (Fig. 3B; Elmore et al., 1967; Woolhouse, 1967). The cot- ton cotyledon maintains a net photosynthetic capability until shortly before the time of abscis- sion (Fig. 3B).

The rate of net photosynthesis per uinit area be- tween 7 and 21 days (Fig. 3) compares well with the rate in 500 ppm CO2 reported by Richardson (1967). He reported a rate of 30 mg C02/dm2/ h, while our results convert to 29.5 mg C02/dm2/ h. (1l 02/cm2/h x 0.1964 = mg C02/dm2/h.) Submergence of the section apparently does not affect photosynthetic rate. In a different applica- tion of the polarographic method, photosynthesis by the cotyledons on seedlings was measured in a small, closed air system. Photosynthetic rates of 28 mg CO2/dm2/h were observed in that applica- tion (Lane, 1977a).

The results of treatments to determine whether transfer of reserves or current photosynthesis plays a predominant role in seedling development seem to permit a straightforward conclusion. Excision of cotyledons often kills the seedling (Lane, 1959) and decidedly delays epicotyl growth. On the other hand, covering with aluminum foil is lethal to neither seedling nor its cotyledons, but also decidedly delays epicotyl growth. The fact that there was no significant decrease in cotyledon dry weight when covered with foil (Table 1) seems to rule out transfer of reserves as a major factor in epicotyl growth. Finally, removal of the terminal bud on a 4-day-old seedling causes a considerable weight accumulation in the cotyledons (Table 1). All of these observations make it highly probable that photosynthesis by the cotyledons provides most of the material and energy necessary for terminal growth.

The functions of cotyledons of cotton and soy- bean provide an interesting comparison. The soy- bean cotyledon undergoes relatively little expan- sion and has a net photosynthetic output less than 5% of that of a cotton cotyledon (cv. Dare, results, this laboratory). The epicotyl of soybean grows rapidly and by 4 days after emergence, the cotyle- dons can be removed with only a relatively slight effect on seedling development (McAlister and Kroher, 1951). Thus, a significant function of soybean cotyledons is the storage and rapid trans- fer of material to the precocious epicotyl. Epicotyl

growth in cotton is comparatively much slower and under adverse field conditions may not be apparent for 2 weeks after emergence. Current photosyn- thesis by the cotyledon is essential to seedling survival under those conditions because little transfer of stored material from the cotyledon occurs in this interval.

The yields and quality of many crops, including cotton, are limited by leaf senescence, which usu- ally occurs while the useful products of the crop plant are developing (Brown et al., 1975). We have attempted to show in this paper that cotton cotyledons will be useful in the study of leaf senescence of cotton because they are the first leaf-like organs produced, their physiological func- tions follow the same pattern as that of the true leaves, and they complete their life in a few weeks. Thus, the time required to grow experimental ma- terial to an appropriate desired stage is much less, thereby providing more opportunity for meaning- ful physiological and biochemical determinations to be made that are needed to elucidate the causes of senescence.

LITERATURE CITED

AMPOFO, S. T., K. G. MOORE, AND P. H. LOVELL. 1976. Cotyledon photosynthesis during seedling develop- ment in Acer. New Phytol. 76: 41-52.

BIALE, J. B. 1975. Fruit ripening and senescence of flowers and leaves. Physiol. Veg. 13: 701-708.

BROWN, A. W. H., T. C. BYERLY, M. GIBBS, AND A. SAN PIETRO. 1975. Crop Productivity. Michigan-Ket- tering Crop Productivity-Research Imperatives. p. 186.

ELMORE, C. D., J. D. HESKETH, AND H. MURAMOTO. 1967. A survey of rates of leaf growth, leaf aging and photosynthetic rates among and within species. J. Ariz. Acad. Sci. 4 #4: 214-219.

EL-SHARKAWY, M., J. HESKETH, AND H. MURAMOTO. 1965. Leaf photosynthetic rates and other growth characteristics among 26 species of Gossypium. Crop Sci. 5: 173-175.

LANE, H. C. 1959. Simulated hail damage experiments in cotton. Tex. Agric. Exp. Stn. Bull. #934.

1977a. Polarographic measurements of respi- ration and photosynthesis by sections of cotton coty- ledons and leaves. Effect of pH, bicarbonate concen- tration, and temperature. Proc. Beltwide Cotton Production Research Conferences, Atlanta, Ga. Na- tional Cotton Council, Memphis, Tenn.

- . 1977b. A rapid procedure for assessing poten- tial net photosynthesis by cotton seedlings. Proc. Beltwide Cotton Production Research Conf. Jan. 1977, Atlanta, Ga. National Cotton Council, Memphis, Tenn.

LOVELL, P. H., AND K. G. MOORE. 1970. A compara- tive study of cotyledons as assimilatory organs. J. Exp. Bot. 21: 1017-1030.

, AND . 1971. A comparative study of the role of the cotyledon in seedling development. J. Exp. Bot. 22: 153-162.

McALISTER, D. F., AND 0. H. KROHER. 1951. Trans- location of food reserves from soybean cotyledons and their influence on the development of the plant. Plant Physiol. 26: 525-538.

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790 AMERICAN JOURNAL OF BOTANY [Vol. 64

RICHARDSON, G. L. 1967. Development of photosyn- thesis in cotton seedlings, Gossy pium hirsutum L. Crop Sci. 7: 6-8.

SASOKI, S., AND T. T. KOZLOWSKI. 1968. The role of cotyledons in early development of pine seedlings. Can. J. Bot. 46: 1173-1183.

WITHROW, R. B. 1957. An interference-filter mono- chromator for irradiation of biological material. Plant Physiol. 32: 355-360.

WOOLHOUSE, H. W. 1967. The nature of senescence in plants: Aspects of the biology of aging. Symp. Soc. Exp. Biol. 21: 179-213.

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