Low growth temperature inhibition of photosynthesis in cotyledons of jack pine seedlings (Pinus banksiana) is due to impaired chloroplast development

Cotyledons of jack pine seedlings (Pinus banksiana Lamb.) grown from seeds were expanded at low temperature (5degreesC), and total Chl content per unit area of cotyledons in these seedlings was only 57% of that observed for cotyledons on 20degreesC-grown controls. Chl a/b ratio of 5degreesC-grown jack pine was about 20% lower (2.3 +/- 0.1) than 20degreesC controls (2.8 +/- 0.3). Separation of Chl-protein complexes and SDS-PAGE indicated a significant reduction in the major Chl a containing complex of PSI (CP1) and PSII (CPa) relative to LHCII1 in 5degreesC compared to 20degreesC-grown seedlings. In addition, LHCII1/LHCII3 ratio increased from 3.8 in control (20degreesC) to 5.5 in 5degreesC-grown cotyledons. Ultrastructurally, 5degreesC-grown cotyledons had chloroplasts with swollen thylakoids as well as etiochloroplasts with distinct prolamellar bodies. Based on CO2-saturated O-2 evolution and in vivo Chl a fluorescence, cotyledons of 5degreesC jack pine exhibited an apparent photosynthetic efficiency that was 40% lower than 20degreesC controls. Seedlings grown at 5degreesC were photoinhibited more rapidly at 5degreesC and 1200 mumol.m(-2).s(-1) than controls grown at 20degreesC, although the final extent of photoinhibition was similar. Exposure to high light at 5degreesC stimulated the xanthophyll cycle in cotyledons of both controls and 5degreesC-grown seedlings. In contrast to winter cereals, we conclude that growth of jack pine at 5degreesC impairs normal chloroplast biogenesis, which leads to an inhibition of photosynthetic efficiency.

[1]  V. Hurry,et al.  Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants , 1993, Photosynthesis Research.

[2]  W. Oberhuber,et al.  Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees , 1991, Planta.

[3]  S. Long,et al.  The occurrence of photoinhibition in an over-wintering crop of oil-seed rape (Brassica napus L.) and its correlation with changes in crop growth. , 1991, Planta.

[4]  G. Öquist,et al.  Light and temperature dependent inhibition of photosynthesis in frost-hardened and un-hardened seedlings of pine , 1989, Photosynthesis Research.

[5]  G. Krause,et al.  Photoinhibition at chilling temperature , 1989, Planta.

[6]  H. Bolhár-Nordenkampf,et al.  Temperature and light dependent modifications of chlorophyll fluorescence kinetics in spruce needles during winter , 1988, Photosynthesis Research.

[7]  J. Williams,et al.  Chloroplast biogenesis at cold-hardening temperatures. Kinetics of trans-Δ3-hexadecenoic acid accumulation and the assembly of LHCII , 1988, Photosynthesis Research.

[8]  E. Ögren,et al.  Effects of winter stress on photosynthetic electron transport and energy distribution between the two photosystems of pine as assayed by chlorophyll fluorescence kinetics , 2004, Photosynthesis Research.

[9]  K. Apel,et al.  Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH-protochlorophyllide oxidoreductase polypeptides in mountain pine (Pinus mugo) , 2004, Planta.

[10]  G. Öquist,et al.  Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis , 2004, Planta.

[11]  G. Krause,et al.  Reversible photoinhibition of unhardened and cold-acclimated spinach leaves at chilling temperatures , 2004, Planta.

[12]  B. Grodzinski,et al.  Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation , 2002 .

[13]  K. Shinohara,et al.  Inhibition of the light-independent synthesis of chlorophyll in pine cotyledons at low temperature. , 2001, Plant & cell physiology.

[14]  G. Öquist,et al.  Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.) , 2001, Planta.

[15]  G. Öquist,et al.  Metabolic Changes During Cold Acclimation and Subsequent Freezing and Thawing , 2001 .

[16]  R. Rikala,et al.  Cold hardiness of Scots pine (Pinus sylvestris L.) , 2001 .

[17]  S. Colombo,et al.  Influence of Nursery Cultural Practices on Cold Hardiness of Coniferous Forest Tree Seedlings , 2001 .

[18]  M. Ball,et al.  Protection and storage of chlorophyll in overwintering evergreens. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Stitt,et al.  Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. , 1999, Plant physiology.

[20]  G. Öquist,et al.  Energy balance and acclimation to light and cold , 1998 .

[21]  T. Repo,et al.  Frost damage and recovery of Scots pine seedlings at the end of the growing season , 1997 .

[22]  F. Sarhan,et al.  Cold Acclimation and Freezing Tolerance (A Complex Interaction of Light and Temperature) , 1997, Plant physiology.

[23]  W. Rüdiger,et al.  The greening process in cress seedlings. V. Possible interference of chlorophyll precursors, accumulated after thujaplicin treatment, with light-regulated expression of Lhc genes , 1996 .

[24]  A. Ivanov,et al.  Photosystem II Excitation Pressure and Development of Resistance to Photoinhibition (II. Adjustment of Photosynthetic Capacity in Winter Wheat and Winter Rye) , 1996, Plant physiology.

[25]  V. Hurry,et al.  LOW-TEMPERATURE STRESS AND PHOTOPERIOD AFFECT AN INCREASED TOLERANCE TO PHOTOINHIBITION IN PINUS-BANKSIANA SEEDLINGS , 1995 .

[26]  W. Rüdiger,et al.  The greening process in cress seedlings IV. Light regulated expression of single Lhc genes , 1995 .

[27]  N. Huner,et al.  Photosystem II Excitation Pressure and Development of Resistance to Photoinhibition (I. Light-Harvesting Complex II Abundance and Zeaxanthin Content in Chlorella vulgaris) , 1995, Plant physiology.

[28]  S. Karpiński,et al.  Developmental Regulation of Light-Independent Transcription of Nuclear- and Plastid-Encoded Chloroplast Proteins in Scots Pine , 1995 .

[29]  D. Campbell,et al.  Seasonal reorganisation of Photosystem II and pigment composition in Pinus sylvestris , 1995 .

[30]  C. Trick,et al.  Growth at Low Temperature Mimics High-Light Acclimation in Chlorella vulgaris , 1994, Plant physiology.

[31]  N. Huner,et al.  A comparison of low temperature growth vs low temperature shifts to induce resistance to photoinhibition in spinach (Spinacia oleracea) , 1994 .

[32]  R. Guy,et al.  Photosynthetic acclimation to low temperature by western red cedar seedlings , 1993 .

[33]  J. Hällgren,et al.  Cold acclimation of Pinus contorta and Pinus sylvestris assessed by chlorophyll fluorescence. , 1993, Tree physiology.

[34]  V. Hurry,et al.  Low-Temperature Effects on Photosynthesis and Correlation with Freezing Tolerance in Spring and Winter Cultivars of Wheat and Rye , 1993, Plant physiology.

[35]  V. Hurry,et al.  Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. , 1992, Plant physiology.

[36]  N. Baker,et al.  Analysis of Light-Induced Depressions of Photosynthesis in Leaves of a Wheat Crop during the Winter. , 1992, Plant physiology.

[37]  N. Yamamoto,et al.  Light-Independent Expression of Three Photosynthetic Genes, cab, rbcS and rbcL, in Coniferous Plants , 1992 .

[38]  J. Williams,et al.  Differential Detergent Stability of the Major Light-Harvesting Complex II in Thylakoids Isolated from Monocotyledonous and Dicotyledonous Plants. , 1992, Plant physiology.

[39]  N. Huner,et al.  Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. , 1992, Plant physiology.

[40]  B. Demmig‐Adams,et al.  Photoprotection and Other Responses of Plants to High Light Stress , 1992 .

[41]  S. Long,et al.  Photoinhibition of holly (Ilex aquifolium) in the field during the winter , 1991 .

[42]  V. Hurry,et al.  Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. , 1991, Plant physiology.

[43]  G. Öquist,et al.  Recovery of photosynthesis in winter‐stressed Scots pine , 1991 .

[44]  A. Gilmore,et al.  Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column , 1991 .

[45]  G. Öquist,et al.  Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and in winter and spring cereals : a fluorescence analysis , 1991 .

[46]  N. Huner,et al.  Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. , 1990, Plant physiology.

[47]  U. Lüttge,et al.  Stress-induced accumulation of the xanthophyll rhodoxanthin in leaves of Aloe vera , 1990 .

[48]  M. Król,et al.  Low Temperature Development under Intermittent Light Conditions Results in the Formation of Etiochloroplasts , 1989 .

[49]  S. Long,et al.  Chlorophyll Fluorescence as a Probe of the Photosynthetic Competence of Leaves in the Field: A Review of Current Instrumentation , 1989 .

[50]  M. Strand,et al.  Effects of frost hardening, dehardening and freezing stress on in vivo chlorophyll fluorescence of seedlings of Scots pine (Pinus sylvestris L.) , 1988 .

[51]  G. Öquist,et al.  A PORTABLE, MICROPROCESSOR OPERATED INSTRUMENT FOR MEASURING CHLOROPHYLL FLUORESCENCE KINETICS IN STRESS PHYSIOLOGY , 1988 .

[52]  T. Lundmark,et al.  Effects of frost on shaded and exposed spruce and pine seedlings planted in the field , 1987 .

[53]  G. Öquist,et al.  Quantum yields of photosynthesis at temperatures between −;2°C and 35°C in a cold‐tolerant C3 plant (Pinus sylvestris) during the course of one year , 1987 .

[54]  R. Rikala,et al.  Frost resistance and frost damage in pinus sylvestris seedlings during shoot elongation , 1987 .

[55]  M. Tollenaar,et al.  Leaf CO2 exchange rates in winter rye grown at cold-hardening and nonhardening temperatures , 1986 .

[56]  M. Strand,et al.  Inhibition of photosynthesis by freezing temperatures and high light levels in cold-acclimated seedlings of Scots pine (Pinus sylvestris). – II. Effects on chlorophyll fluorescence at room temperature and 77 K. , 1985 .

[57]  M. Strand,et al.  Inhibition of photosynthesis by freezing temperatures and high light Levels in cold‐acclimated seedlings of Scots pine (Pinus sylvestris). ‐ I. Effects on the light‐limited and light‐saturated rates of CO2 assimilation , 1985 .

[58]  M. Król,et al.  Growth and development at cold-hardening temperatures. Chloroplast ultrastructure, pigment content, and composition , 1984 .

[59]  G. Öquist,et al.  Effects of artificial frost hardening and winter stress on net photosynthesis, photosynthetic electron transport and RuBP carboxylase activity in seedlings of Pinus silvestris , 1980 .

[60]  M. Król The Relationship between Photosynthetic Activities and the Polypeptide Pattern of Pine Seedling Chloroplasts , 1978 .

[61]  B. Gunning,et al.  Plant Cell Biology: An Ultrastructural Approach , 1976 .

[62]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[63]  D. Arnon COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.