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Effect of heat shock on ultrastructure and calcium distribution in Lavandula pinnata L. glandular trichomes

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Abstract

The effects of heat shock (HS) on the ultrastructure and calcium distribution of Lavandula pinnata secretory trichomes are examined using transmission electron microscopy and potassium antimonate precipitation. After 48-h HS at 40°C, plastids become distorted and lack stroma and osmiophilic deposits, the cristae of the mitochondria become indistinct, the endoplasmic reticulum acquires a chain-like appearance with ribosomes prominently attached to the lamellae, and the plasma and organelle membranes become distorted. Heat shock is associated with a decrease in calcium precipitates in the trichomes, while the number of precipitates increases in the mesophyll cells. Prolonged exposure to elevated calcium levels may be toxic to the mesophyll cells, while the lack of calcium in the glands cell may deprive them of the normal protective advantages of elevated calcium levels. The inequality in calcium distribution may result not only from uptake from the transpiration stream, but also from redistribution of calcium from the trichomes to the mesophyll cells.

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References

  • Abdelmageed AHA, Grudaz N (2007) Influence of heat shock pretreatment on growth and development of tomatoes under controlled heat stress conditions. J Appl Bot Food Qual 81:26–28

    Google Scholar 

  • Amelunxen F, Gronau G (1968) Elektronenmikroskopische untersuchungen an den Olzellen von Acorus calamus L. Z Pflanzenphysiol 60:156–168

    Google Scholar 

  • Antunes T, Sevinate-Pinto I (1991) Glandular trichomes of Teucrium scorodonia L. morphology and histochemistry. Flora 185:65–70

    Google Scholar 

  • Biyaseheva AE, Molotkovskii YG, Mamonov LK (1993) Increase of free Ca2+ in the cytosol of plant protoplasts in response to heat stress as related to Ca2+ homeostasis. Russian J Plant Physiol 40:540–544

    Google Scholar 

  • Blum A (1996) Plant breeding for stress environments. CRC, Boca Raton

    Google Scholar 

  • Burstrom HG (1968) Calcium and plant growth. Bio Rev 43:287–316

    Article  CAS  Google Scholar 

  • Boudsocq M, Sheen J (2010) Stress signaling II: calcium sensing and signaling. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer, Dordrecht, pp 75–90

    Google Scholar 

  • Boursiac Y, Lee SM, Romanowsky S, Blank R, Sladek C, Chung WS, Harper JF (2010) Disruption of the vacuolar calcium-ATPases in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant Physiol 154:1158–1171

    Article  PubMed  CAS  Google Scholar 

  • Bramm J (1992) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc Natl Acad Sci USA 89:3213–3216

    Article  Google Scholar 

  • Bush DS (1995) Calcium regulation in plants cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46:95–122

    Article  CAS  Google Scholar 

  • Canny MJ (1990) What becomes of the transpiration stream? New Phytol 114:341–368

    Article  Google Scholar 

  • Ciamporova M, Mistrik I (1993) The ultrastructural response of root cells to stressful conditions. Environ Exp Bot 33:11–26

    Article  Google Scholar 

  • Clapham DE (1995) Calcium signaling. Cell 80:259–268

    Article  PubMed  CAS  Google Scholar 

  • Collins GG, Nie XL, Saltveit ME (1995) Heat-shock proteins and chilling sensitivity of mung bean hypocotyls. J Exp Bot 46:795–802

    Article  CAS  Google Scholar 

  • Colorado P, Rodriguez A, Nicolas G, Rodriguez D (1994) Abscisic acid and stress regulate gene expression during germination of chick-pea seeds. Possible role of calcium. Physiol Plantarum 91:461–467

    Article  CAS  Google Scholar 

  • De Silva DLR, Hetheringtion AM, Mansfield TA (1996) Where does all the calcium go? Evidence of an important regulatory role for trichomes in two calcicoles. Plant Cell Environ 19:880–886

    Article  Google Scholar 

  • Gersbach PV (2002) The essential oil secretory structures of Prostanthera ovalifolia (Lamiaceae). Ann Bot 89:255–260

    Article  PubMed  CAS  Google Scholar 

  • Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771

    Article  PubMed  CAS  Google Scholar 

  • Gong M, Li YJ, Dai X, Tian M, Li ZG (1997) Involvement of calcium and calmodulin in the acquisition of heat-shock induced thermotolerance in maize. J Plant Physiol 150:615–621

    Article  CAS  Google Scholar 

  • Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437

    Article  CAS  Google Scholar 

  • Hepler PK, Wayne RO (1985) Calcium and plant development. Ann Rev Plant Physiol 36:397–439

    Article  CAS  Google Scholar 

  • Huang SS, Kirchoff BK, Liao JP (2008) The capitate and peltate glandular trichomes of Lavandula pinnata L. (Lamiaceae): histochemistry, ultrastructure and secretion. J Torrey Bot Soc 135:155–167

    Article  Google Scholar 

  • Huang SS, Liao JP, Kirchoff BK (2010) Calcium distribution and function in glandular trichomes of Lavandula pinnata L. (Lamiaceae). J Torrey Bot Soc 137:1–15

    Article  Google Scholar 

  • Jian LC, Li JH, Chen WP, Paul HL, Ahlstrand GG (1999) Cytochemical localization of calcium and Ca2+-ATPase activity in plant cells under chilling stress: a comparative study between the chilling-sensitive maize and the chilling-insensitive winter wheat. Plant Cell Physiol 40:1061–1071

    Article  CAS  Google Scholar 

  • Jiang YW, Huang BG (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52:341–349

    Article  PubMed  CAS  Google Scholar 

  • Karley AJ, Leigh RA, Sanders D (2000) Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends Plant Sci 5:465–470

    Article  PubMed  CAS  Google Scholar 

  • Kiang JG, Carr FE, Burns MR, McClain DE (1994) HSP-72 synthesis is promoted by increase in [Ca2+]i or activation of G proteins but not pHi or cAMP. Am J Physiol–Cell Physiol 267:104–114

    Google Scholar 

  • Klein JD, Ferguson IB (1987) Effect of high temperature on calcium uptake by suspension-cultured pear fruit cells. Plant Physiol 84:153–156

    Article  PubMed  CAS  Google Scholar 

  • Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov VV, Andreev IM, Trofimova MS (1998) The synthesis of HSPs in sugar beet suspension culture cells under hyperthermia exhibits differential sensitivity to calcium. Biochem Mol Biol Int 45:269–278

    PubMed  CAS  Google Scholar 

  • Leigh RA, Tomos AD (1993) Ion distribution in cereal leaves: pathways and mechanisms. Philos Trans Royal Soc Lond B Biol Sci 341:75–86

    Article  CAS  Google Scholar 

  • Li B, Liu HT, Sun DY, Zhou RG (2004) Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant cell Physiol 45:627–634

    Article  PubMed  CAS  Google Scholar 

  • Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132:1186–1195

    Article  PubMed  CAS  Google Scholar 

  • Lynch DV, Lepock JR, Thompson JE (1987) Temperature-induced changes in lipid fluidity alter the conformation of proteins in senescing plant membranes. Plant cell Physiol 28:787–797

    CAS  Google Scholar 

  • Ma XD, Wang L, Wang M, Peng H (2003) Difference in relative conductivity and ultrastructure of leaf between two wheat cultivars with different thermotolerance under heat acclimation and heat stress. Journal of China Agricultural University 8:4–8 (in Chinese)

    Google Scholar 

  • Miao C, Li RQ, Wang JB (1994) Ultrastructural study in leaf cell of Brassica oleracea var. capitata under heat stress. Acta Bot Sinica 36:730–732, in Chinese

    Google Scholar 

  • Minorsky PV (1985) A heuritic hypothesis of chilling injury in plants: a role for calcium as primary physiological transducer of injury. Plant Cell Environ 8:75–94

    Article  CAS  Google Scholar 

  • Mistrik M, Holobrada M, Ciapporova M (1992) The root in unfavourable conditions. In: Kolek J, Kozinka V (eds) Physiology of plant root system. Kluwer Academic, Dordrecht, pp 286–312

    Google Scholar 

  • Mosser DD, Kotzbauer PT, Sarge KD, Morimoto RI (1990) In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc Natl Acad Sci U S A 87:3748–3752

    Article  PubMed  CAS  Google Scholar 

  • Nicotera P, Zhivotovsky B, Orrenius S (1994) Nuclear calcium transport and the role of calcium in apoptosis. Cell Calcium 16:279–288

    Article  PubMed  CAS  Google Scholar 

  • Palta JP (1990) Stress interactions at the cellular and membrane levels. Hortic science 25:1377–1381

    CAS  Google Scholar 

  • Pareek A, Singla S, Grover A (1997) Short-term salinity and high temperature stress-associated ultrastructural alterations in young leaf cells of Oryza sativa L. Ann Bot 80:629–639

    Article  Google Scholar 

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Enviro Exp Bot 69:225–232

    Article  Google Scholar 

  • Santarius KA, Weis E (1988) Heat stress and membranes. In: Plant membranes—structure, assembly and function. Biochem Soc, pp 97-112

  • Simon EW (1978) The symptoms of calcium deficiency in plants. New Phytology 80:1–15

    Article  CAS  Google Scholar 

  • Singla SL, Pareek A, Grover A (1997) High temperature. In: Prasad MNV (ed) Plant ecophysiology. Wiley, New York, pp 101–127

    Google Scholar 

  • Slocum RD, Roux SJ (1982) An improved method for the subcellular localization of calcium using a modification of the antimonate precipitates technique. J Histochem Cytochem 30:617–629

    Article  PubMed  CAS  Google Scholar 

  • Starck Z, Siwiec A, Chotuj D (1994) Distribution of calcium in tomato plants in response to heat stress and plant growth regulators. Plant Soil 167:143–148

    Article  CAS  Google Scholar 

  • Steponkus PL (1981) Responses to extreme temperatures: cellular and sub-cellular bases. In: Lange OL, Nobel PS, Osmond CB, Ziegier H (ed) Physiological plant ecology: responses to the physical environment. Springer, New York, 12: 372-402

  • Tian HQ, Russell SD (1997) Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L. Planta 202:93–105

    Article  CAS  Google Scholar 

  • Tian HQ, Zhu H, Russell SD (2000) Calcium changes in ovules and embryo sacs of Plumbago zeylanica L. Sex Plant Rep 13:11–20

    Article  CAS  Google Scholar 

  • Trofimova MS, Andreev IM, Kuznetsov VV (1999) Calcium is involved in regulation of the synthesis of HSPs in suspension-cultured sugar beet cells under hyperthermia. Physiol Plant 105:67–73

    Article  CAS  Google Scholar 

  • Turner GW, Gershenzon J, Croteau RB (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–680

    Article  PubMed  CAS  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Ann Rev Plant Physiol Plant Mol Biol 42:579–602

    Article  CAS  Google Scholar 

  • Wang GY, Liu JM, Zhang Y, Yu BS, Shen ZY (1997) Studies on ultrastructure in common bean leaves during heat acclimation and heat stress. J Agric Biotech 7:151–156 (in Chinese)

    Google Scholar 

  • Wang JB, Li RQ (1999) Changes of Ca2+ distribution in mesophyll cells of pepper under heat stress. Acta Hortic Sinca 26:57–58

    Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Webb AAR, Mcainsh MR, Taylor JE, Hetherington AM (1996) Calcium ions as intracellular second messenger in higher plants. Adv Bot Res 22:45–96

    Article  CAS  Google Scholar 

  • Werker E (1993) Function of essential oil-secreting glandular hairs in aromatic plants of the Lamiaceae—a review. Flavor Fragr J 8:249–255

    Article  Google Scholar 

  • White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899

    Article  PubMed  CAS  Google Scholar 

  • Wick SM, Hepler PK (1980) Localization of Ca 2+-containing antimonate precipitations during mitosis. J Cell Biol 86:500–513

    Article  PubMed  CAS  Google Scholar 

  • Yan CL, Wang JB, Li RQ (2002) Effect of heat stress on calcium ultrastructural distribution in pepper anther. Environ Exp Bot 48:161–168

    Article  CAS  Google Scholar 

  • Zhang ZS, Li RQ, Wang JB (2000) Effect of Ca2+, La3+ and EGTA treatment on the responses of pepper leaves to heat stress. J Wuhan Univ 46:253–256 (in Chinese)

    CAS  Google Scholar 

  • Zhao HJ, Tan JF (2005) Role of calcium ion in protection against heat and high irradiance stress-induced oxidative damage to photosynthesis of wheat leaves. Photosynthetica 43:473–476

    Article  CAS  Google Scholar 

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Acknowledgments

The first author thanks Xu, XingLan and Hu, XiaoYing, instructors in the Electron Microscopy facility of the South China Botanical Garden, for their assistance in learning EM. We also thank two anonymous reviewers for their helpful comments on the manuscript.

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The authors declare that they have no conflicts of interest.

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Correspondence to S. S. Huang.

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Handling Editor: Alexander Schulz

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Huang, S.S., Kirchoff, B.K. & Liao, J.P. Effect of heat shock on ultrastructure and calcium distribution in Lavandula pinnata L. glandular trichomes. Protoplasma 250, 185–196 (2013). https://doi.org/10.1007/s00709-012-0393-7

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  • DOI: https://doi.org/10.1007/s00709-012-0393-7

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