Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T18:02:01.599Z Has data issue: false hasContentIssue false

Important metabolic pathways in poultry embryos prior to hatch

Published online by Cambridge University Press:  12 November 2008

J.E. DE OLIVEIRA
Affiliation:
North Carolina State University, Department of Poultry Science, Raleigh, NC, USA 27695
Z. UNI
Affiliation:
Hebrew University, Faculty of Agriculture, Department of Animal Science, Rehovot, Israel 76100
P.R. FERKET*
Affiliation:
North Carolina State University, Department of Poultry Science, Raleigh, NC, USA 27695
*
Corresponding author: [email protected]
Get access

Abstract

Growth performance and meat yield of commercial broilers and turkeys has improved linearly each year during the past four decades (Havenstein et al., 2003b; Havenstein et al., 2003a; Havenstein et al., 2007), and this trend is likely to continue in the future as new technologies in genetics, biotechnology and developmental biology are adopted by the poultry industry. As the time it takes meat birds to achieve market size decreases, the period of embryonic development becomes a greater proportion of a bird's productive life. Therefore, incubation and embryonic development towards hatch is of greater relative importance to the successful rearing of meat poultry than ever before (Hulet 2007; Foye et al., 2007b). Consequently, anything that supports or limits growth and development during the incubation period will have a marked effect on overall growth performance and health of modern strains of meat poultry. Many poultry researchers now realize that future gains in genetic and production potential of poultry will come from advancements made during the incubation period and embryogenesis (Elibol et al., 2002; Peebles et al., 2005; Christensen et al., 2007; Collin et al., 2007; Leksrisompong et al., 2007). The urgent need to explore and understand the biology of incubation has been emphasised by several symposia: two held at the annual conference of the U.S. Poultry Science Society (July 2006-Edmonton, Alberta, Canada “Managing the embryo for performance”, and July 2007-San Antonio, TX Informal Nutrition Meeting “The impact of imprinting on biological and economical performance in animals”), and one held by the European Federation of World Poultry Science Society (October 2007-Berlin, Germany “Fundamental physiology and perinatal development in poultry), which were specifically devoted to demonstrating the importance of the embryonic period on poultry performance. This review will summarise the metabolic events and pathways in four of the most active tissues of embryos during the period just prior to hatch, and the hormonal control that coordinates the marked changes as the embryo prepares for its post-hatch life.

Type
Review Article
Copyright
Copyright © World's Poultry Science Association 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

APPLEGATE, T.J., KARCHER, D.M. and LILBURN, M.S. (2005) Comparative development of the small intestine in the turkey poult and Pekin duckling. Poultry Science 84: 426-431.CrossRefGoogle ScholarPubMed
BAKHUIS, W.L. (1974) Observations on hatching movements in the chick (Gallus domesticus). Journal of Comparative Physiology and Psychology 87: 997-1003.Google Scholar
BAUMANN, R. and MEUER, H.J. (1992) Blood oxygen transport in the early avian embryo. Physiological Reviews 72: 941-965.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L. and BIELLIER, H.V. (1982) Physiology of turkey embryos during pipping and hatching. IV. Thyroid function in embryos from selected hens. Poultry Science 61: 2482-2488.Google Scholar
CHRISTENSEN, V.L., BIELLIER, H.V. and FORWARD, J.F. (1982) Physiology of turkey embryos during pipping and hatching III. Thyroid function. Poultry Science 61: 367-374.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L., DONALDSON, W.E. and MCMURTRY, J.P. (1996) Physiological differences in late embryos from turkey breeders at different ages. Poultry Science 75: 172-178.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L., DONALDSON, W.E. and NESTOR, K.E. (1999) Length of the plateau and pipping stages of incubation affects the physiology and survival of turkeys. British Poultry Science 40: 297-303.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L., WINELAND, M.J., FASENKO, G.M. and DONALDSON, W.E. (2001) Egg storage effects on plasma glucose and supply and demand tissue glycogen concentrations of broiler embryos. Poultry Science 80: 1729-1735.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L., GRIMES, J.L., WINELAND, M.J. and DAVIS, G.S. (2003a) Accelerating embryonic growth during incubation following prolonged egg storage. 2. Embryonic growth and metabolism. Poultry Science 82: 1869-1878.CrossRefGoogle ScholarPubMed
CHRISTENSEN, V.L., ORT, D.T. and GRIMES, J.L. (2003b) Physiological factors associated with weak neonatal poults (Meleagris gallopavo). International Journal of Poultry Science 2: 7-14.Google Scholar
CHRISTENSEN, V.L., ORT, D.T., NESTOR, K.E., VELLEMAN, S.G. and HAVENSTEIN, G.B. (2007) Genetic control of neonatal growth and intestinal maturation in turkeys. Poultry Science 86: 476-487.CrossRefGoogle ScholarPubMed
COLLIN, A., BERRI, C., TESSERAUD, S., RODON, F.E., SKIBA-CASSY, S., CROCHET, S., DUCLOS, M.J., RIDEAU, N., TONA, K., BUYSE, J., BRUGGEMAN, V., DECUYPERE, E., PICARD, M. and YAHAV, S. (2007) Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens. Poultry Science 86: 795-800.Google Scholar
DONALDSON, W.E. and CHRISTENSEN, V.L. (1991) Dietary carbohydrate level and glucose metabolism in turkey poults. Comparative Biochemistry and Physiology A 98: 347-350.CrossRefGoogle ScholarPubMed
DONALDSON, W.E., CHRISTENSEN, V.L. and KRUEGER. K.K., (1991) Effects of stressors on blood glucose and hepatic glycogen concentrations in turkey poults. Comparative Biochemistry and Physiology A 100: 945-947.Google Scholar
DONALDSON, W.E. (1995) Carbohydrate, hatchery stressors affect poult survival. Feedstuffs 67(14): 16-17.Google Scholar
ELIBOL, O., PEAK, S.D. and BRAKE, J. (2002) Effect of flock age, length of egg storage, and frequency of turning during storage on hatchability of broiler hatching eggs. Poultry Science 81: 945-950.CrossRefGoogle ScholarPubMed
FEHER, G. (1988) The process of hatching in geese and ducks. Anatomia, Histologia, Embryologia 17: 107-120.Google ScholarPubMed
FOYE, O.T. (2005) The biochemical and molecular effects of amnionic nutrient administration, “in ovo feeding” on intestinal development and function and carbohydrate metabolism in turkey embryos and poults. Ph.D. Dissertation. North Carolina State University. Raleigh, NC.Google Scholar
FOYE, O.T., UNI, Z. and FERKET, P.R. (2006) Effect of in ovo feeding egg white protein, beta-hydroxy-beta-methylbutyrate, and carbohydrates on glycogen status and neonatal growth of turkeys. Poultry Science 85: 1185-1192.CrossRefGoogle ScholarPubMed
FOYE, O.T., FERKET, P.R. and UNI, Z. (2007a) The effects of in ovo feeding arginine, beta-hydroxy-beta-methyl-butyrate, and protein on jejunal digestive and absorptive activity in embryonic and neonatal turkey poults. Poultry Science 86: 2343-2349.CrossRefGoogle ScholarPubMed
FOYE, O.T., FERKET, P.R. and UNI, Z. (2007b) Ontogeny of energy and carbohydrate utilisation of the precocial avian embryo and hatchling. Avian and Poultry Biology Reviews 18(3): 93-101.CrossRefGoogle Scholar
GEORGE, J.C. and BERGER, A.J. (1966) Avian myology Academic Press, New York.Google Scholar
GEYRA, A., UNI, Z. and and SKLAN, D. (2001) Enterocyte dynamics and mucosal development in the posthatch chick. Poultry Science 80: 776-782.Google Scholar
GILBERT, E.R., LI, H., EMMERSON, D.A., WEBB JR., K.E. and WONG, E.A. (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poultry Science 86: 1739-1753.CrossRefGoogle ScholarPubMed
GROSS, G.H. (1985) Innervation of the complexus ("hatching") muscle of the chick. Journal of Comparative Neurology 232: 180-189.CrossRefGoogle ScholarPubMed
HAVENSTEIN, G.B., FERKET, P.R. and QURESHI, M.A. (2003a) Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82: 1500-1508.Google Scholar
HAVENSTEIN, G.B., FERKET, P.R. and QURESHI, M.A. (2003b) Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82: 1509-1518.CrossRefGoogle ScholarPubMed
HAVENSTEIN, G.B., FERKET, P.R., GRIMES, J.L., QURESHI, M.A. and NESTOR, K.E. (2007) Comparison of the performance of 1966- versus 2003-type turkeys when fed representative 1966 and 2003 turkey diets: growth rate, livability, and feed conversion. Poultry Science 86: 232-240.CrossRefGoogle ScholarPubMed
HULET, R.M. (2007) Managing incubation: where are we and why? Poultry Science 86: 1017-1019.Google Scholar
JEHLE, P.M., FUSSGAENGER, R.D., BLUM, W.F., ANGELUS, N.K., HOEFLICH, A., WOLF, E. and JUNGWIRTH, R.J. (1999) Differential autocrine regulation of intestine epithelial cell proliferation and differentiation by insulin-like growth factor (IGF) system components. Hormone and Metabolic Research 31: 97-102.Google Scholar
JOHN, T.M., GEORGE, J.C. and MORAN JR., E.T. (1987) Pre- and post-hatch ultrastructural and metabolic changes in the hatching muscle of turkey embryos from antibiotic and glucose treated eggs. Cytobios 49: 197-210.Google ScholarPubMed
JOHN, T.M., GEORGE, J.C. and MORAN JR., E.T. (1988) Metabolic changes in pectoral muscle and liver of turkey embryos in relation to hatching: influence of glucose and antibiotic-treatment of eggs. Poultry Science 67: 463-469.CrossRefGoogle ScholarPubMed
JOULIA, D., BERNARDI, H., GARANDEL, V., RABENOELINA, F., VERNUS, B. and CABELLO, G. (2003) Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Experimental Cell Research 286(2): 263-275CrossRefGoogle ScholarPubMed
KARCHER, D.M., MCMURTRY, J.P. and APPLEGATE, T.J. (2005) Developmental changes in amniotic and allantoic fluid insulin-like growth factor (IGF)-I and -II concentrations of avian embryos. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 142: 404-409.Google Scholar
KATANBAF, M.N., DUNNINGTON, E.A. and SIEGEL, P.B. (1988) Allomorphic relationships from hatching to 56 days in parental lines and F1 crosses of chickens selected 27 generations for high or low body weight. Growth, Development, and Aging 52: 11-21.Google ScholarPubMed
KEIRS, R.W., PEEBLES, E.D., HUBBARD, S.A. and WHITMARSH, S.K. (2002) Effects of supportative gluconeogenic substrates on early performance of broilers under adequate brooding conditions. Journal of Applied Poultry Research 11: 367-372.Google Scholar
KREBS, H.A. (1972) Some aspects of the regulation of fuel supply in omnivorous animals. Advances in Enzyme Regulation 10: 397-420.Google Scholar
KUCERA, P., RADDATZ, E. and BAROFFIO, A. (1984) Oxygen and glucose uptake in the early chick embryo. In: R.S. SEYMOUR and JUNK, W. (Eds) Respiration and Metabolism of Embryonic Vertebrates. pp. 299-309 (Dordrecht, The Netherlands).Google Scholar
LANGLEY, B., THOMAS, M., BISHOP, A., SHARMA, M., GILMOUR, S. and KAMBADUR, R. (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. The Journal of Biological Chemistry 277: 49831-49840CrossRefGoogle ScholarPubMed
LANGSLOW, D.R., CRAMB, G. and SIDDLE, K. (1979) Possible mechanisms for the increased sensitivity to glucagon and catecholamines of chicken adipose tissue during hatching. General and Comparative Endocrinology 39: 527-533.CrossRefGoogle ScholarPubMed
LEKSRISOMPONG, N., ROMERO-SANCHEZ, H., PLUMSTEAD, P.W., BRANNAN, K.E. and BRAKE, J. (2007) Broiler incubation. 1. Effect of elevated temperature during late incubation on body weight and organs of chicks. Poultry Science 86: 2685-2691.Google Scholar
LU, J.W., MCMURTRY, J.P. and COON, C.N. (2007) Developmental changes of plasma insulin, glucagon, insulin-like growth factors, thyroid hormones, and glucose concentrations in chick embryos and hatched chicks. Poultry Science 86: 673-683.Google Scholar
MATTHEWS, C.K. and HOLDE, K.E. (1990a) Carbohydrate metabolism I: anaerobic processes in generating metabolic energy. In: Biochemistry. pp. 670-703 (The Benjamin/Cummnings Publishing Company, Inc., Redwood City, CA).Google Scholar
MATTHEWS, C.K. and HOLDE, K.E. (1990b) Metabolism of nitrogenous compounds: principles of biosynthesis, utilization, turnover, and excretion. In: Biochemistry. pp. 670-703 (The Benjamin/Cummings Publishing Company, Inc., Redwood City, CA).Google Scholar
MATTHEWS, C.K. and HOLDE, K.E. (1990c) Integration and control of Metabolic processes. In: Biochemistry. pp. 779-814 (The Benjamin/Cummnings Publishing Company, Inc., Redwood City, CA).Google Scholar
MCMURTRY, J.P., ROSEBROUGH, R.W., BROCHT, D.M, FRANCIS, G.L., UPTON, Z. and PHELPS, P. (1998) Assessment of developmental changes in chicken and turkey insulin-like growth factor-II by homologous radioimmunoassay. The Journal of Endocrinology 157: 463-473.CrossRefGoogle ScholarPubMed
MORAN JR., E.T. (2007) Nutrition of the developing embryo and hatchling. Poultry Science 86: 1043-1049.Google Scholar
MORAN, L.A. (1994) Lipid metabolism. In: L.A. MORAN (Ed) Biochemistry. pp. 20.21-20.14 (Neil Patterson/Prentice Hall, Englewood Cliffs, NJ).Google Scholar
MURAMATSU, T., HIRAMOTO, K., KOSHI, N., OKUMURA, J., MIYOSHI, S. and MITSUMOTO, T. (1990) Importance of albumen content in whole-body protein synthesis of the chicken embryo during incubation. British Poultry Science 31: 101-106.CrossRefGoogle ScholarPubMed
NOBIKUNI, K., KOGA, K.O. and NISHIYAMA, H. (1989) The effects of thyroid hormones on liver glycogen, muscle glycogen and liver lipids in chicks. Japanese Journal of Zootechnical Science 60: 346-348.Google Scholar
PEARCE, J. and BROWN, W.O. (1971) Carbohydrate metabolism (Academic Press, London).Google Scholar
PEEBLES, E.D., KEIRS, R.W., BENNETT, L.W., CUMMINGS, T.S., WHITMARSH, S.K. and GERARD, P.D. (2005) Relationships among prehatch and posthatch physiological parameters in early nutrient restricted broilers hatched from eggs laid by young breeder hens. Poultry Science 84: 454-461.CrossRefGoogle ScholarPubMed
PHILLIPS, R.E. and WILLIAMS, C.S. (1943) External morphology of the turkey during the incubation period. Poultry Science 22: 270-277.Google Scholar
PICARDO, M. and DICKSON, A.J. (1982) Hormonal regulation of glycogen metabolism in hepatocyte suspensions isolated from chicken embryos. Comparative biochemistry and physiology. B, Comparative biochemistry 71: 689-693.Google Scholar
REDDY, D.V., LOMBARDO, M.E. and CERECEDO, L.R. (1952) Nucleic acid changes during the development of the chick embryo. The Journal of Biological Chemistry 198: 267-270.CrossRefGoogle ScholarPubMed
ROMANOFF, A.L. (1960) The avian embryo; structural and functional development (Macmillian, New York, NY).Google Scholar
ROMANOFF, A.L. (1967) Biochemistry of the avian embryo; a quantitative analysis of prenatal development (Interscience Publishers, New York).Google Scholar
SATO, M., TACHIBANA, T. and FURUSE, M. (2006) Heat production and lipid metabolism in broiler and layer chickens during embryonic development. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 143: 382-388.Google Scholar
SCOTT, T.R., JOHNSON, W.A., SATTERLEE, D.G. and GILDERSLEEVE, R.P. (1981) Circulating levels of corticosterone in the serum of developing chick embryos and newly hatched chicks. Poultry Science 60: 1314-1320.CrossRefGoogle ScholarPubMed
SELL, J.L., ANGEL, C.R., PIQUER, F.J., MALLARINO, E.G. and AL-BATSHAN, H.A. (1991) Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poultry Science 70: 1200-1205.Google Scholar
SMAIL, J.R. (1964) A possible role of the Musculus complexus in pipping the chicken egg. The American midland naturalist 72: 499-506.Google Scholar
TAKO, E., FERKET, P.R. and UNI, Z. (2004) Effects of in ovo feeding of carbohydrates and beta-hydroxy-beta-methylbutyrate on the development of chicken intestine. Poultry Science 83: 2023-2028.Google Scholar
TAYLOR, W.E., BHASIN, S., ARTAZA, J., BYHOWER, F., AZAM, M. and WILLARD, D.H. (2001) Myostatin inhibits cell proliferation and protein synthesis in c2C12 muscle cells. American journal of physiology. Endocrinology and metabolism 280: E221-E228.Google Scholar
UNI, Z., NOY, Y. and SKLAN, D. (1999) Posthatch development of small intestinal function in the poult. Poultry Science 78: 215-222.Google Scholar
UNI, Z., GEYRA, A., BEN-HUR, H. and SKLAN, D. (2000) Small intestinal development in the young chick: crypt formation and enterocyte proliferation and migration. British Poultry Science 41: 544-551.Google Scholar
UNI, Z., TAKO, E., GAL-GARBER, O. and SKLAN, D. (2003) Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo. Poultry Science 82: 1747-1754.Google Scholar
UNI, Z. and FERKET, P.R. (2004) Methods for early nutrition and their potential. World´s Poultry Science Journal 60: 101-111.CrossRefGoogle Scholar
UNI, Z., FERKET, P.R., TAKO, E. and KEDAR, O. (2005) In ovo feeding improves energy status of late-term chicken embryos. Poultry Science 84: 764-770.CrossRefGoogle ScholarPubMed
VELLEMAN, S.G. (2007) Muscle development in the embryo and hatchling. Poultry Science 86: 1050-1054.Google Scholar
WARNER, J.D., FERKET, P.R., CHRISTENSEN, V.L. and FELTS, J.V. (2006) Effect of season, hatch time, and post-hatch holding on glycogen status of turkey poults. Poultry Science 85(Suppl. 1): 117 (Abstr.).Google Scholar
ZHOU, H., EVOCK-CLOVER, C.M., MCMURTRY, J.P., ASHWELL, C.M. and LAMONT, S.J. (2007) Genome-wide linkage analysis to identify chromosomal regions affecting phenotypic traits in the chicken. IV. Metabolic traits. Poultry Science 86: 267-276.CrossRefGoogle ScholarPubMed