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Ultrastructure and functional activity of chloroplasts in wheat leaves under root chilling

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Abstract

The effects of root chilling (2 °C; during 1, 5 h, 1, 2, 4 and 7 days) on the ultrastructure, functional activity of chloroplasts and cold tolerance of leaf cells of wheat (Triticum aestivum L.) were studied. Results indicated that the area of the chloroplasts increased and the number of grana in the chloroplast decreased already within first hours of the experiment. On the 2nd–7th day of the cold treatment, the length of photosynthetic membranes in the chloroplasts increased owing to the membranes of thylakoids in grana. The number of chloroplasts per cell was increased by the end of the experiment. Reduction of electron transport rate and intensification of non-photochemical quenching of chlorophyll fluorescence were observed in the first hours of root chilling. The growth of the leaves slowed in the first day of the treatment and resumed on the second day. Leaf area in the root-chilled plants by the end of the experiment exceeded the initial values by 60 %. The significant rise in cold tolerance of leaf cells was detected after 24 h of root chilling. After 48 h of the treatment, the cold tolerance reached a maximum, and did not change thereafter. It is assumed that most of the observed structural and functional changes are adaptive, and meant to support the photosynthetic function and promote the cold tolerance of the plants.

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Abbreviations

ETR:

Electron transport rate

qN:

Coefficient of non-photochemical quenching

Chl:

Chlorophyll

Car:

Carotenoids

LT50 :

Temperature lethal to 50 % of palisade parenchyma cells

References

  • Aldridge C, Maple J, Møller SG (2005) The molecular biology of plastid division in higher plants. J Exp Bot 56:1061–1077

    Article  CAS  PubMed  Google Scholar 

  • Al-Hamdani SH, Thomas TS (2000) Influence of root chilling on winter and spring wheat growth and carbon dioxide assimilation. Acta Agric Scand 50:149–154

    Google Scholar 

  • Aroca R, Tognoni F, Irigoyen JJ, Sanches-Dias M, Pardossi A (2001) Different root low temperature response of two maize genotypes differing in chilling sensitivity. Plant Physiol Biochem 39:1067–1073

    Article  CAS  Google Scholar 

  • Artuso A, Guidi L, Soldatini GF, Pardossi A, Tognoni F (2000) The influence of chilling on photosynthesis and activities of some enzymes of sucrose metabolism in Lycopersicon esculentum Mill. Acta Physiol Plant 22:95–101

    Article  CAS  Google Scholar 

  • Balagurova NI, Akimova TV, Titov AF (2001) The effect of local cooling of cucumber and wheat seedlings on various kinds of stress resistance of their leaves and roots. Russ J Plant Physiol 48:95–99

    Article  CAS  Google Scholar 

  • Bigot J, Boucaud J (2006) Short-term responses of Brassica rapa plants to low temperature: effects of nitrate uptake and its translocation to the shoot. Physiol Plant 96:646–654

    Article  Google Scholar 

  • Bloom AJ, Zvieniecki MA, Passioura JB, Randal LB, Holbrook NM, Clair D (2004) Water relations under root chilling in a sensitive and tolerant tomato species. Plant Cell Environ 27:971–980

    Article  Google Scholar 

  • Buchner O, Holzinger A, Lütz C (2007) Effects of temperature and light on the formation of chloroplasts protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ 30:1347–1356

    Article  CAS  PubMed  Google Scholar 

  • Chazen O, Neumann PM (1994) Hydraulic signals from the roots and rapid cell-wall hardening in growing maize (Zea mays L.) leaves are primary response to polyethylene glycol-induced water deficit. Plant Physiol 104:1385–1392

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cui H, Ma W, Hu J, Li Y, Zheng Y (2012) Chilling tolerance evaluation and physiological and ultrastructural changes under chilling stress in tobacco. Afr J Agric Res 7:3349–3359

    Google Scholar 

  • Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  PubMed  Google Scholar 

  • Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • From J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469

    Article  Google Scholar 

  • Fromm J, Lauther S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    Article  CAS  PubMed  Google Scholar 

  • Garbero M, Andrade A, Reinoso H, Fernández B, Cuesta C, Granda V, Escudero C, Abdala G, Pedranzani H (2012) Differential effect of short-term cold stress on growth, anatomy, and hormone levels in cold-sensitive versus resistance cultivars of Digiteria eriantha. Acta Physiol Plant. doi:10.1007/s11738-012-1007-x

  • Herde O, Pena-Cortes H, Fuss H, Willmitzer L, Fisahn J (1999) Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants. Physiol Plant 105:144–179

    Article  Google Scholar 

  • Hola D, Kutik J, Kocova M, Rothova O (2008) Low-temperature induced changes in the ultrastructure of maize mesophyll chloroplasts strongly depend on the chilling pattern/intensity and considerably differ among inbred and hybrid genotypes. Photosynthetica 46:329–338

    Article  CAS  Google Scholar 

  • Hurry VM, Strand A, Tobiason M, Gardestöm P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol 109:697–706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jeschke W, Hartung W (2000) Root-shoot interactions in mineral nutrition. Plant Soil 226:57–69

    Article  CAS  Google Scholar 

  • Jeschke WD, Holodbrata M, Hartung W (1997) Growth of Zea mays L. plants with their seminal roots only. Effects of plant development, xylem transport, mineral nutrition and the flow and distribution of abscisic acid (ABA) as a possible shoot to root signal. J Exp Bot 48:1229–1239

    Article  CAS  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • Kutik J, Hola D, Kocova M, Rothova O, Haise D, Wilhelmova N, Ticha I (2004) Ultrastructure and dimensions of chloroplasts in leaves of three maize (Zea mays L.) inbred lines and their F1 hybrids grown under moderate chilling stress. Photosynthetica 42:447–455

    Article  Google Scholar 

  • Lee SH, Singh AD, Chung GC, Ahn SJ, Noh EK, Stendie E (2004) Exposure of roots of cucumber (Cucumus sativus) to low temperature severely reduced root pressure, hydraulic conductivity and active transport of nutrients. Physiol Plant 120:413–422

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Wellburn AL (1983) Determination of total carotenoids and chlorophylls a and b of leaf exacts in different solvents. Biochem Soc Trans 11:591–593

    CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio Rfd of leaves with the PAM fluorimeter. Photosynthetica 43:379–393

    Article  CAS  Google Scholar 

  • Luo HY, Lee SK, He J (2009) Integrated effects of root-zone temperatures and phosphorus levels on aeroponically-grown lettuce (Lactuca sativa L.) in the tropics. Open Hortic J 2:6–12

    Article  CAS  Google Scholar 

  • Lütz C, Engel L (2007) Changes of chloroplasts ultrastructure in some light-alpine plants: adaptation to metabolic demands and climate. Protoplasma 231:183–192

    Article  PubMed  Google Scholar 

  • Ma SF, Lin CY, Chen YM (1990) Comparative studies of chilling stress on alterations of chloroplast ultrastructure and protein synthesis in the leaves of chilling-sensitive (mungbean) and––insensitive (pea) seedlings. Bot Bull Acad Sin 31:263–272

    Google Scholar 

  • Macduff JH, Hopper MJ, Wild A (1987) The effect of root temperature of growth and uptake of ammonium and nitrate by Brassica napus L. cv. Bien venu in flowing solution culture. II. Uptake from solution containing NH4NO3. J Exp Bot 38:53–66

    Article  CAS  Google Scholar 

  • Malone M (1993) Rapid inhibition of leaf growth by root chilling in wheat: kinetics and mechanisms. J Exp Bot 44:505–510

    Article  Google Scholar 

  • Maxwell K, Johnson G (2000) Chlorophyll fluorescence––a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • McCully ME (1999) Root xylem embolism and refilling. Relation to water potentials of soil, roots, and leaves, and osmotic potentials of root xylem sap. Plant Physiol 119:1001–1008

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mishra NS, Mallick BN, Sopory SK (2001) Electrical signal from root to shoot in Sorghum bicolor: induction of leaf opening and evidence for fast extracellular propagation. Plant Sci 160:237–245

    Article  CAS  PubMed  Google Scholar 

  • Miyasaka SC, Grunes DL (1997) Root zone temperature and calcium effects on phosphorus, sulfur, and micronutrients in winter wheat forage. Agron J 89:743–748

    Article  Google Scholar 

  • Musser RL, Thomas SA, Kramer PJ (1983) Short and long effects of root and shoot chilling of Ransome. Soybean Plant Physiol 73:778–783

    Article  CAS  Google Scholar 

  • Rapacz M, Gasior D, Zweirzykowski Z, Lesniewska-Bolianovska A, Humphreys MW, Gay AP (2004) Changes in cold tolerance and the mechanisms of acclimation of photosystem II to cold hardening generated by anther culture of Festuca pratensis × Lolium multifolium cultivars. New Phytol 162:105–114

    Article  CAS  Google Scholar 

  • Sicher RC, Timlin D, Bailey B (2012) Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J Plant Physiol 169:686–695

    Article  CAS  PubMed  Google Scholar 

  • Siddiqi MY, Memon AR, Glass ADM (1984) Regulation of K+ influx in barley: effects of low temperature. Plant Physiol 74:730–734

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith PG, Dale JE (1988) The effects of root cooling and excision treatments on the growth of primary leaves of Phaseolus vulgaris L. Rapid and reversible increases in abscisic acid content. New Phytol 110:293–300

    Article  Google Scholar 

  • Talanova VV, Titov AF, Topchieva LV, Malysheva IE, Venzhik YV, Nazarkina EA (2010) Gene expression in wheat leaves under local exposure of roots to a low temperature. Doklady Biol Sci 435:438–440

    Article  CAS  Google Scholar 

  • Ternesi M, Andrade AP, Jorrin J, Benlloch M (1994) Root-shoot signaling in sunflower plants with confined root system. Plant Soil 166:31–36

    Article  CAS  Google Scholar 

  • Titov AF, Talanova VV, Akimova TV (2003) The effect of root treatment with various stress agents of plant cold- and heat-tolerance. Russ J Plant Physiol 50:94–99

    Article  Google Scholar 

  • Vella GF, Joss TV, Roberts TH (2012) Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming. Protoplasma 249:1137–1149

    Article  CAS  PubMed  Google Scholar 

  • Venzhik YV, Titov AF, Talanova VV, Frolova SA, Talanov AV, Nazarkina EA (2011) Influence of lowered temperature on the resistance and functional activity of the photosynthetic apparatus of wheat plants. Biol Bull 38:132–137

    Article  CAS  Google Scholar 

  • Venzhik YV, Titov A, Talanova VV, Miroslavov EA, Koteeva NK (2013) Structural and functional reorganization of the photosynthetic apparatus in adaptation to cold of wheat plants. Cell Tissue Biol 7:168–176

    Article  Google Scholar 

  • Veselova S, Farhutdinov R, Mitrichenko A, Symonyan M, Hartung W (2003) The effect of root cooling on hormone content and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.). Bulg J Plant Physiol, special Issue: 360–366

  • Veselova S, Farhutdinov R, Veselov DS, Kudoyarova GR (2006) Role of cytokinins in the regulation of stomatal conductance of wheat seedlings under conditions of rapidly changing local temperature. Russ J Plant Physiol 53:857–862

    Google Scholar 

  • Wang G, Guo Z (2005) Effect of chilling stress on photosynthetic rate and chlorophyll fluorescence parameter in seedlings of two rice cultivars differing in cold tolerance. Rice Sci 12:187–191

    Google Scholar 

  • Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O′Donnel PJ, Bowles DJ (1992) Electrical signaling and systemic proteinase inhibition in the wounded plant. Nature 360:62–65

    Article  CAS  Google Scholar 

  • Yamasaki T, Yamakawa T, Yamane Yo, Koike H, Satoh K, Katoh S (2002) Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiol 128:1087–1097

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ye Z, Bell RW, Dell B, Huang L (2000) Response of sunflower to boron supply at low root zone temperature. Comm Soil Plant Anal 31:2379–2392

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Karelian Research Centre, Institute of Biology, Russian Academy of Sciences, 11 Pushkinskaya St., 185910, Petrozavodsk, Russia

    Yu. V. Venzhik, A. F. Titov & V. V. Talanova

  2. Komarov Botanical Institute, Russian Academy of Sciences, 2 Popov Av., 197376, St. Petersburg, Russia

    E. A. Miroslavov

Authors
  1. Yu. V. Venzhik
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  2. A. F. Titov
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  3. V. V. Talanova
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  4. E. A. Miroslavov
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Correspondence to Yu. V. Venzhik.

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Communicated by U. Feller.

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Venzhik, Y.V., Titov, A.F., Talanova, V.V. et al. Ultrastructure and functional activity of chloroplasts in wheat leaves under root chilling. Acta Physiol Plant 36, 323–330 (2014). https://doi.org/10.1007/s11738-013-1413-8

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  • DOI: https://doi.org/10.1007/s11738-013-1413-8

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