STEREOLOGY, AN UNBIASED METHODOLOGICAL APPROACH TO STUDY PLANT ANATOMY AND CYTOLOGY: PAST, PRESENT AND FUTURE
DOI:
https://doi.org/10.5566/ias.1848Keywords:
chloroplast, confocal microscopy, leaf anatomy, mesophyll, stereological methods, systematic uniform random samplingAbstract
This review presents an historical overview of stereological methods used for the quantitative evaluation of plant anatomical and cytological structures. It includes the origins of these methods up to the most recent developments such as the application of stereology based on 3D images. We focus especially on leaf, as the vast majority of studies of plant microscopic structure examine this organ. An overview of plant cell ultrastructure measurements as well as plant anatomical characteristics (e.g. plant tissue volume density, internal leaf surface area, number and mean size of mesophyll cells and chloroplast number), which were estimated by stereological methods most frequently, is presented. We emphasize the importance of proper sampling needed for unbiased measurements. Furthermore, we mention other methods used for plant morphometric studies and briefly discuss their relevance, precision, unbiasedness and efficiency in comparison with unbiased stereology. Finally, we discuss reasons for the sparse use of stereology in plant anatomy and consider the future of stereology in plant research.
References
Adachi S, Nakae T, Uchida M, Soda K, Takai T, Oi T, Yamamoto T, Ookawa T, Miyake H, Yano M (2013). The mesophyll anatomy enhancing CO2 diffusion is a key trait for improving rice photosynthesis. J Exp Bot 64:1061–72.
Albertsson P, Andreasson E (2004). The constant proportion of grana and stroma lamellae in plant chloroplasts. Physiol Plantarum 121:334–42.
Albrechtová J (1994). Quantitative analysis of leaves of sun and shade ecotypes of Solanum dulcamara L. Acta Stereol 13:467-72.
Albrechtová J, Janáček J, Lhotáková Z, Radochová B, Kubínová L (2007). Novel efficient methods for measuring mesophyll anatomical characteristics from fresh thick sections using stereology and confocal microscopy: application on acid rain-treated Norway spruce needles. J Exp Bot 58:1451–61.
Albrechtová J, Kubínová L (1991). Quantitative analysis of the structure of etiolated barley leaf using stereological methods. J Exp Bot 42:1311–14.
Albrechtová J, Kubínová L, Votrubová O, Eliášová K (1998). Non-destructive stereological method for estimating the length of rigid root systems. Biol Plantarum 40:311–6.
Baddeley A, Gundersen H-JG, Cruz-Orive LM (1986). Estimation of surface area from vertical sections. J Microsc-Oxford 142:259–76.
Barbour M, Farquhar G (2004). Do pathways of water movement and leaf anatomical dimensions allow development of gradients in H218O between veins and the sites of evaporation within leaves? Plant Cell Environ 27:107–21.
Bernardo S, Dinisa L-T, Luzio A, Pinto G, Meijón M, Valledor L, Conde A, Gerós H, Correia CM, Moutinho-Pereira J (2017). Kaolin particle film application lowers oxidative damage and DNA methylation on grapevine (Vitis vinifera L.). Env Exp Bot 139:39–47.
Bertel C, Schönswetter P, Frajman B, Holzinger A, Neuner G (2017). Leaf anatomy of two reciprocally non-monophyletic mountain plants (Heliosperma spp.): does heritable adaptation to divergent growing sites accompany the onset of speciation? Protoplasma 254:1411–20.
Boardman N (1977). Comparative photosynthesis of sun and shade plants. Ann Rev Plant Physio 28:355–77.
Bockers M, Čapková V, Tichá I, Schäfer C (1997). Growth at high CO2 affects the chloroplast number but not the photosynthetic efficiency of photoautotrophic Marchantia polymorpha culture cells. Plant Cell Tiss Org 48:103–10.
Boffey SA, Ellis JR, Selldén G, Leech RM (1979). Chloroplast division and DNA synthesis in light-grown wheat leaves. Plant Physiol 64:502–5.
Bondada BR, Syvertsen JP (2003). Leaf chlorophyll, net gas exchange and chloroplast ultrastructure in citrus leaves of different nitrogen status. Tree Physiol 23:553–9.
Bray S, Reid DM (2002). The effect of salinity and CO2 enrichment on the growth and anatomy of the second trifoliate leaf of Phaseolus vulgaris. Can J Botany 80:349–59.
Buffon GLL (1777). Essai d´arithmétique morale. In: Histoire naturelle, générale et particulière: servant de suite à la théorie de la terre, & d’introduction à l’histoire des minéraux. De l’imprimerie royale, Paris, pp 46–148.
Bunce JA, Patterson DT, Peet MM, Alberte RS (1977). Light acclimation during and after leaf expansion in soybean. Plant Physiol 60:255–8.
Burundukova O, Zhuravlev YN, Solopov N, P’yankov V (2003). A method for calculating the volume and surface area in rice mesophyll cells. Russian Journal of Plant Physiol 50:133–9.
Byott G (1976). Leaf air space systems in C3 and C4 species. New Phytol 76:295–9.
Chabot BF, Chabot JF (1977). Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26:363–77.
Charles-Edwards DA, Charles-Edwards J, Sant F (1972). Models for mesophyll cell arrangement in leaves of ryegrass (Lolium perenne L.). Planta 104:297–305.
Charles-Edwards DA, Charles-Edwards J, Sant F (1974). Leaf photosynthetic activity in six temperate grass varieties grown in contrasting light and temperature environments. J Exp Bot 25:715–24.
Chonan N (1965). Studies on the photosynthetic tissues in the leaves of cereal crops. I. The mesophyll structure of wheat leaves inserted at different levels of the shoot. Proc Crop Sci Soc Jpn 33:388–93.
Chonan N (1966). Studies on the photosynthetic tissues in the leaves of cereal crops. II. Effect of shading on the mesophyll structure of the wheat leaves. Proc Crop Sci Soc Jpn 35:78–82.
Chonan N (1970). Studies on the photosynthetic tissues in the leaves of cereal crops. V. Comparison of the mesophyll structure among seedling leaves of cereal crops. Proc Crop Sci Soc Jpn 39:418–25.
Coate JE, Luciano AK, Seralathan V, Minchew KJ, Owens TG, Doyle JJ (2012). Anatomical, biochemical, and photosynthetic responses to recent allopolyploidy in Glycine dolichocarpa (Fabaceae). Am J Bot 99:55–67.
Crumpton-Taylor M, Grandison S, Png KM, Bushby AJ, Smith AM (2012). Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol 158:905–16.
Cruz-Orive LM, Howard CV (1991). Estimating the length of a bounded curve in three dimensions using total vertical projections. J Microsc-Oxford 163:101–13.
Czerski J (1968). Gasometric method of water deficit measurement in leaves. Biol Plantarum 10:275–83.
Demmig-Adams B, Muller O, Stewart JJ, Cohu CM, Adams WW (2015). Chloroplast thylakoid structure in evergreen leaves employing strong thermal energy dissipation. J Photoch Photobio B 152:357–66.
Dengler NG, MacKay LB (1975). The leaf anatomy of beech, Fagus grandifolia. Can J Botany 53:2202–11.
Dinkins R, Reddy SM, Leng M, Collins GB (2001). Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta 214:180–8.
Dornhoff GM, Shibles R (1976). Leaf morphology and anatomy in relation to CO2-exchange rate of soybean leaves. Crop Sci 16:377–81.
Eames AJ, MacDaniels LH (1925). An Introduction to Plant Anatomy. McGraw-Hill Book Co. Inc., New York, pp. 321–42.
Edwards SJ, Isaac S, Collin HA, Clipson NJ (1999). Stereological analysis of celery leaves infected by Septoria apiicola. Mycol Res 103:750–6.
Eleftheriou E (1987). A comparative study of the leaf anatomy of olive trees growing in the city and the country. Environ Exp Bot 27:105–17.
Ellis J, Leech R (1985). Cell size and chloroplast size in relation to chloroplast replication in light-grown wheat leaves. Planta 165:120–5.
El-Sharkawy MA, Hesketh J (1965). Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistances. Crop Sci 5:517–21.
El-Sharkawy MA (2009). Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems. Photosynthetica 47:163-83.
Fagerberg W (1983). A quantitative study of daily variation in the cellular ultrastructure of palisade chlorenchyma from sunflower leaves. Ann Bot-London 52:117–26.
Fagerberg WR, Bornman JF (1997). Ultraviolet-B radiation causes shade-type ultrastructural changes in Brassica napus. Physiol Plantarum 101:833–44.
Flood PJ, Kruijer W, Schnabel SK, van der Schoor R, Jalink H, Snel JFH, Harbinson J, Aarts MGM (2016). Phenomics for photosynthesis, growth and reflectance in Arabidopsis thaliana reveals circadian and long-term fluctuations in heritability. Plant Methods 12:14.
Gabarayeva NI, Grigorjeva VV (2002). Exine development in Stangeria eriopus (Stangeriaceae): ultrastructure and substructure, sporopollenin accumulation, the equivocal character of the aperture, and stereology of microspore organelles. Rev Palaeobot Palyno 122:185–218.
Gamalei YuV, Kulikov GV (1978). Razvitie khlorenkhimy lista. [Development of leaf chlorenchyma.]. Nauka, Leningrad.
Gao H, Sage TL, Osteryoung KW (2006). FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. P Natl Acad Sci-Biol 103:6759–64.
Gopi R, Jaleel CA, Panneerselvam R (2008). Leaf anatomical responses of Amorphophallus campanulatus to triazoles fungicides. Eurasia J Biosci 2, 46-52.
Gowland A, Briarty LG, Davey MR (1987). Tobacco leaf structure-an analytical problem. Acta Stereol 6:497–502.
Gregoriou K, Pontikis K, Vemmos S (2007). Effects of reduced irradiance on leaf morphology, photosynthetic capacity, and fruit yield in olive (Olea europaea L.). Photosynthetica 45:172–81.
Griffin KL, Anderson OR, Gastrich MD, Lewis JD, Lin G, Schuster W, Seemann JR, Tissue DT, Turnbull MH, Whitehead D (2001). Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure. P Natl Acad Sci-Biol 98:2473–8.
Gundersen HJG, Jensen E (1987). The efficiency of systematic sampling in stereology and its prediction. J Microsc-Oxford 147:229–63.
Gundersen HJG (1986). Stereology of arbitrary particles - a review of unbiased number and size estimators and the presentation of some new ones, in memory of Thompson,William, R. J Microsc-Oxford 143:3–45.
Hajibagheri M, Hall J, Flowers T (1984). Stereological analysis of leaf cells of the halophyte Suaeda maritima (L.) Dum. J Exp Bot 35:1547–57.
Hayashida A, Takechi K, Sugiyama M, Kubo M, Itoh R, Takio S, Fujita T, Hiwatashi Y, Hasebe M, Takano H (2005). Isolation of mutant lines with decreased numbers of chloroplasts per cell from a tagged mutant library of the moss Physcomitrella patens. Plant Biol 7:300–6.
Holá D, Kutík J, Kočová M, Rothová 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 46:329–38.
Howard CV, Reed MG (1998). Unbiased stereology: three-dimensional measurement in microscopy. Springer, New York.
Howard CV, Sandau K (1992) Measuring the surface area of a cell by the method of the spatial grid with a CSLM – a demonstration. J Microsc 165: 183-88.
Howard V, Reid S, Baddeley A, Boyde A (1985). Unbiased estimation of particle density in the tandem scanning reflected light microscope. J Microsc-Oxford 138:203–12.
Ivanova L, P’yankov V (2002). Structural adaptation of the leaf mesophyll to shading. Russian Journal of Plant Physiol 49:419–31.
James SA, Smith WK, Vogelmann TC (1999). Ontogenetic differences in mesophyll structure and chlorophyll distribution in Eucalyptus globulus ssp. globulus (Myrtaceae). Am J Bot 86:198–207.
Jellings AJ, Leech RM (1984). Anatomical variation in first leaves of nine Triticum genotypes, and its relationship to photosynthetic capacity. New Phytol 96:371–82.
Jin B, Wang L, Wang J, Jiang K-Z, Wang Y, Jiang X-X, Ni C-Y, Wang Y-L, Teng N-J (2011). The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in Arabidopsis thaliana. BMC Plant Biol 11:35.
Juurola E, Aalto T, Thum T, Vesala T, Hari P (2005). Temperature dependence of leaf‐level CO2 fixation: revising biochemical coefficients through analysis of leaf three‐dimensional structure. New Phytol 166: 205-15.
Khramtsova E, Kiseleva I, Lyubomudrova E, Malkova N (2003). Optimization of the leaf mesophyll structure in alloploid and diploid wheat species. Russian journal of Plant Physiol 50:19–27.
Kivimäenpää M, Sutinen S, Karlsson PE, Selldén G (2003). Cell structural changes in the needles of Norway spruce exposed to long‐term ozone and drought. Ann Bot-London 92:779-93.
Kivimäenpää M, Riikonen J, Sutinen S, Holopainen T (2014). Cell structural changes in the mesophyll of Norway spruce needles by elevated ozone and elevated temperature in open-field exposure during cold acclimation. Tree Physiol 34:389–403.
Klich MG (2000). Leaf variations in Elaeagnus angustifolia related to environmental heterogeneity. Environ Exp Bot 44:171–83.
Konoplyova A, Petropoulou Y, Yiotis C, Psaras GK, Manetas Y (2008). The fine structure and photosynthetic cost of structural leaf variegation. Flora-Morphology, Distribution, Functional Ecology of Plants 203:653–62.
Kubínová L (1987). Application of stereological methods to the anatomy of the leaf blade of barley. Acta Stereol 6:99–104.
Kubínová L (1989a). Stereological analysis of the leaf of barley. Acta Stereol 8:19–26.
Kubínová L (1989b). Effect of light intensity on anatomical structure of the leaf blade of barley: Stereological analysis. Acta Stereol 8:389–94.
Kubínová L (1991). Stomata and mesophyll characteristics of barley leaf as affected by light: stereological analysis. J Exp Bot 42:995–1001.
Kubínová L (1993). Recent stereological methods for the measurement of leaf anatomical characteristics: estimation of volume density, volume and surface area. J Exp Bot 44:165–73.
Kubínová L (1994). Recent stereological methods for measuring leaf anatomical characteristics: estimation of the number and sizes of stomata and mesophyll cells. J Exp Bot 45:119–27.
Kubínová L (1998). Stereology in plant anatomy: application of recent stereological principles to evalution of plant cells. Fol Anat 26 (Suppl.1).:1–7.
Kubínová L, Janáček J (1998). Estimating surface area by the isotropic fakir method from thick slices cut in an arbitrary direction. J Microsc-Oxford 191:201–11.
Kubínová L, Janáček J (2001). Confocal microscopy and stereology: Estimating volume, number, surface area and length by virtual test probes applied to three-dimensional images. Microsc Res Techniq 53:425–35.
Kubínová L, Janáček J (2015). Confocal stereology: an efficient tool for measurement of microscopic structures. Cell Tissue Res 360:13–28.
Kubínová L, Janáček J, Albrechtová J, Karen P (2005). Stereological and digital methods for estimating geometrical characteristics of biological structures using confocal microscopy. In: Evangelista V, Barsanti L, Passarelli V, Gualtieri P (eds). From Cells to Proteins: Imaging Nature across Dimensions. Springer, pp 271–321.
Kubínová L, Janáček J, Guilak F, Opatrný Z (1999). Comparison of several digital and stereological methods for estimating surface area and volume of cells studied by confocal microscopy. Cytometry 36:85–95.
Kubínová L, Janáček J, Karen P, Radochová B, Difato F, Krekule I (2004). Confocal stereology and image analysis: methods for estimating geometrical characteristics of cells and tissues from three-dimensional confocal images. Physiol Res 53:S47-56.
Kubínová L, Janáček J, Krekule I (2002). Stereological methods for estimating geometrical parameters of microscopical structure studied by three-dimensional microscopical techniques. In: Diaspro A (ed). Confocal and Two-photon Microscopy. Wiley-Liss, New York, pp 299–332.
Kubínová L, Kutík J (2007). Surface density and volume density measurements of chloroplast thylakoids in maize (Zea mays L.) under chilling conditions. Photosynthetica 45:481–8.
Kubínová Z, Janáček J, Lhotáková Z, Kubínová L, Albrechtová J (2014). Unbiased estimation of chloroplast number in mesophyll cells: advantage of a genuine three-dimensional approach. J Exp Bot 65:609–20.
Kukkola E, Rautio P, Huttunen S (2005). Long-term symptoms due to metal and acid precipitation treatments in Scots pine (Pinus sylvestris). needles in the subarctic. Arct Antarct Alp Res 37:68–74.
Kutík J, Nátr L, Demmers-Derks H, Lawlor DW (1995). Chloroplast ultrastructure of sugar beet (Beta vulgaris L.) cultivated in normal and elevated CO2 concentrations with two contrasted nitrogen supplies. J Exp Bot 46:1797–802.
Kutík J, Šesták Z, Volfová A (1984) Ontogenetic changes in the internal limitations to bean-leaf photosynthesis. VIII: Primary leaf blade characteristics and chloroplast number, size and ultrastructure. Photosynthetica 18:1–8.
Lamppa GK, Elliot LV, Bendich AJ (1980). Changes in chloroplast number during pea leaf development. Planta 148:437–43.
Lepeduš H, Cesar V, Ljubesic N (2001). Chloroplast ultrastructure and chlorophyll levels in vegetative buds and needles of Norway spruce (Picea abies L. Karst.). Period Biol 103(1): 61-5.
Lhotáková Z, Albrechtová J, Janáček J, Kubínová L (2008). Advantages and pitfalls of using free-hand sections of frozen needles for three-dimensional analysis of mesophyll by stereology and confocal microscopy. J Microsc-Oxford 232:56–63.
Lhotáková Z, Urban O, Dubánková M, Cvikrová M, Tomášková I, Kubínová L, Zvára K, Marek MV, Albrechtová J (2012). The impact of long-term CO2 enrichment on sun and shade needles of Norway spruce (Picea abies).: Photosynthetic performance, needle anatomy and phenolics accumulation. Plant Sci 188:60–70.
Lieckfeldt E (1989). Importance of leaf anatomy for characterization of primary leaf photosynthetic efficiency in different genotypes of wheat (Triticum). Photosynthetica 23:63–70.
Liu Y, Dengler NG (1994). Bundle sheath and mesophyll cell differentiation in the C4 dicotyledon Atriplex rosea: quantitative ultrastructure. Can J Botany 72:644–57.
Longstreth DJ, Bolaños JA, Goddard RH (1985). Photosynthetic rate and mesophyll surface area in expanding leaves of Alternanthera philoxeroides grown at two light levels. Am J Bot 72:14–9.
Lukjanova A, Mandre M, Saarman G (2013). Impact of alkalisation of the soil on the anatomy of Norway spruce (Picea abies) needles. Water Air Soil Poll 224:1620.
Luković J (2006). Stereological analysis of the flag leaf of some Triticum L. species. Cereal Res Commun 34:1005–12.
Luković J, Zorić L, Piperac J, Nagl N, Karanović D, Kekić SM, Milić D (2016). The analysis of petiole histological traits through an evaluation of water deficit tolerance of sugar beet genotypes. Sugar Tech 18:160–7.
Luković J, Kraljević-Balalić M, Vujičić D (2001). Characteristics of the flag leaf vascular tissue in two Triticum species. Cereal Res Commun 29: 151–8.
Maksymowych R (1959). Quantitative analysis of leaf development in Xanthium pensylvanicum. Am J Bot 46:635–44.
Maksymowych R (1963). Cell division and cell elongation in leaf development of Xanthium pensylvanicum. Am J Bot 50:891–901.
Marin M, Koko V, Duletić-Laušević S, Marin PD (2008). Micromorphology of trichomes of Thymus malyi (Lamiaceae). J Microsc-Oxford 232:406–9.
Marin M, Koko V, Duletić-Laušević S, Marin PD, Rančić D, Dajić-Stevanović Z (2006). Glandular trichomes on the leaves of Rosmarinus officinalis: Morphology, stereology and histochemistry. S Afr J Bot 72:378–82.
Marrison JL, Rutherford SM, Robertson EJ, Lister C, Dean C, Leech RM (1999). The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J 18:651–62.
Mašková P, Radochová B, Lhotáková Z, Michálek J, Lipavská H (2017). Nonstructural carbohydrate-balance response to long-term elevated CO2 exposure in European beech and Norway spruce mixed cultures: biochemical and ultrastructural view. Can J Forest Res 47:1488-94.
Maslova T, Mamushina N, Sherstneva O, Bubolo L, Zubkova E (2009). Seasonal structural and functional changes in the photosynthetic apparatus of evergreen conifers. Russ J Plant Phys 56:607–15.
Meyer FJ (1923). Das trophische Parenchym. A. Assimilationsgewebe. In: Handbuch der Pflanzenanatomie. Allgemeiner Teil: Histologie (Linsbauer K, ed.), 2nd edn. Berlin, Bd. 5, 1. Hälfte: pp 1–87.
Meyer R, Yuan J, Afzal J, Iqbal M, Zhu M, Garvey G, Lightfoot DA (2006). Identification of Gsr1 in Arabidopsis thaliana: a locus inferred to regulate gene expression in response to exogenous glutamine. Euphytica 151:291–302.
Miroslavov EA, Voznesenskaya EV, Bubolo LS (1996). Chloroplast structure in northern plants in relation to chloroplast adaptation to arctic conditions. Russian Journal of Plant Physiol 43:325–30.
Miyazawa S, Terashima I (2001). Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant Cell Environ 24:279–91.
Molin WT, Meyers SP, Baer GR, Schrader LE (1982). Ploidy effects in isogenic populations of Alfalfa II. Photosynthesis, chloroplast number, ribulose-1,5-bisphosphate carboxylase, chlorophyll, and DNA in protoplasts. Plant Physiol 70:1710-4.
Morris P, Thain J (1983). Improved methods for the measurement of total cell surface area in leaf mesophyll tissue. J Exp Bot 34:95–8.
Morrod R (1974). A new method for measuring the permeability of plant cell membranes using epidermis-free leaf discs. J Exp Bot 25:521–33.
Moura BB, Alves ES (2014) Climatic factors influence leaf structure and thereby affect the ozone sensitivity of Ipomoea nil ‘Scarlet O’Hara.’ Environ Pollut 194:11–6.
Mozafari J, Wolyn D, Ali-Khan S (1997). Chromosome doubling via tuber disc culture in dihaploid potato as determined by confocal microscopy. Plant Cell Rep 16:329–33.
Nátr L (1988). Quantitative anatomy of plants. Acta U Carol Biol 31:5–13.
Newman E (1966). A method of estimating the total length of root in a sample. J Appl Ecol 139–45.
Niinemets U (2007). Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–71.
Nius E (1931). Untersuchungen über den Einfluß des Interzellularvolumens und der Öffnungsweite der Stomata auf die Luftwegigkeit der Laubblätter. Jb Wiss Bot 74:33–126.
Nobel PS, Zaragoza LJ, Smith WK (1975). Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiol 55:1067–70.
Oguchi R, Hikosaka K, Hirose T (2003). Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–12.
Oguchi R, Hikosaka K, Hirose T (2005). Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–27.
Oksanen E, Sober J, Karnosky D (2001). Impacts of elevated CO2 and/or O3 on leaf ultrastructure of aspen (Populus tremuloides). and birch (Betula papyrifera). in the Aspen FACE experiment. Environ Pollut 115:437–46.
Paolillo Jr DJ, Falk RH (1966). The ultrastructure of grana in mesophyll plastids of Zea mays. Am J Bot 173–80.
Parker M, Ford M (1982). The structure of the mesophyll of flag leaves in three Triticum species. Ann Bot-London 49:165–76.
Parkhurst DF (1982). Stereological methods for measuring internal leaf structure variables. Am J Bot 69:31–9.
Pawley JB (1995). Handbook of biological confocal microscopy, 2nd edn. Plenum Press, New York.
Pawley JB (2006). Handbook of Biological Confocal Microscopy, 3rd edn. Springer US, Boston, MA.
Pazourek J (1966). Anatomical gradients. Acta U Carol Biol Suppl. 1/2:19–25.
Pazourek J (1969). Anatomical gradients of stomatal apparatus in leaves of Hordeum distichon L. Adv Front Pl Sci 23:9–18.
Pazourek J (1975). Transversale anatomische Gradienten in der Kartoffelknolle. Biol Plantarum 17:263–7.
Pazourek J (1977). The volumes of anatomical components in leaves of Typha angustifolia L. and Typha latifolia L. Biol Plantarum 19:129–35.
Pazourek J (1988). The evolution of quantitative plant anatomy. Acta Univ Carol, Biol 31:15–25.
Pazourek J, Nátr L (1981). Changes in the anatomical structure of the first two leaves of barley caused by the absence of nitrogen or phosphorus in the nutrient medium. Biol Plantarum 23:296–301.
Pazourek J, Nátr L, Marková L (1987). Genotype differences in the proportion of different tissues in the leaves of spring barley. Biol Plantarum 29:54–62.
Pechová R, Kutík J, Holá D, Kočová M, Haisel D, Vičánková A (2003). The ultrastructure of chloroplasts, content of photosynthetic pigments, and photochemical activity of maize (Zea mays L.) as influenced by different concentrations of the herbicide amitrole. Photosynthetica 41:127–36.
Perktold A, Zellnig G, Guttenberger H, Gailhofer M (1998). 3D reconstruction of chloroplasts and their ultrastructure using ultra-thin-serial-sections. Phyton-Horn- 38:159–66.
Peterson DA (1999). Quantitative histology using confocal microscopy: implementation of unbiased stereology procedures. Methods 18:493–507.
Possingham JV, Saurer W (1969). Changes in chloroplast number per cell during leaf development in spinach. Planta 86:186–94.
Possingham JV, Smith JW (1972). Factors affecting chloroplast replication in spinach. J Exp Bot 23:1050–9.
Pritchard S, Peterson C, Prior S, Rogers H (1997). Elevated atmospheric CO2 differentially affects needle chloroplast ultrastructure and phloem anatomy in Pinus palustris: interactions with soil resource availability. Plant Cell Environ 20:461–71.
Pyke KA, Leech RM (1991). Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol 96:1193–5.
Razem FA, Davis AR (1999). Anatomical and ultrastructural changes of the floral nectary of Pisum sativum L. during flower development. Protoplasma 206:57–72.
Ren B, Liu W, Zhang J, Dong S, Liu P, Zhao B (2017). Effects of plant density on the photosynthetic and chloroplast characteristics of maize under high-yielding conditions. Sci. Nat. 104:12.
Rhizopoulou S, Psaras GK (2003). Development and structure of drought‐tolerant leaves of the mediterranean shrub Capparis spinosa L. Ann Bot-London 92:377–383.
Riikonen J, Oksanen E, Peltonen P, Holopainen T, Vapaavuori E (2003). Seasonal variation in physiological characteristics of two silver birch clones in the field. Can J Forest Res 33:2164–76.
Salisbury E (1928). On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos T R Soc Lon B 216:1–65.
Sam O, Ramírez C, Coronado M, Testillano P, Risueño M del C (2003). Changes in tomato leaves induced by NaCl stress: leaf organization and cell ultrastructure. Biol Plantarum 47:361–6.
Sant F (1969). A comparison of the morphology and anatomy of seedling leaves of Lolium multiflorum Lam. and L. perenne L. Ann Bot-London 33:303–13.
Sasahara T (1971). Genetic Variations in Cell and Tissue Forms in Relation to Plant Growth.: II. Total Cell Surface Area in the Palisade Parenchyma and Total Cell Surface Area: Total Nitrogen Content Ratio in Relation to Photosynthetic Activity in Brassica. Jpn J Breed 21:61–8.
Sasahara T (1982). Influence of genome on leaf anatomy of Triticum and Aegilops. Ann Bot-London 50:491–7.
Sawidis TH, Eleftheriou EP, Tsekos I (1989). The floral nectaries of Hibiscus rosa-sinensis in. A morphometric and ultrastructural approach. Nord J Bot 9:63–71.
Schmitt V, Kußmaul A, Wild A (1999). Interaction of elevated CO2 and ozone concentrations and irrigation regimes on leaf anatomy and carbohydrate status of young oak (Quercus petraea) trees. Z Naturforsch C 54:812–23.
Simon UK, Polanschütz LM, Koffler BE, Zechmann B (2013). High resolution imaging of temporal and spatial changes of subcellular ascorbate, glutathione and H2O2 distribution during Botrytis cinerea infection in Arabidopsis. PLoS One 8:e65811.
Slaton MR, Smith WK (2002). Mesophyll architecture and cell exposure to intercellular air space in alpine, desert, and forest species. Int J Plant Sci 163:937–48.
Slavík B (1963). The distribution pattern of transpiration rate, water saturation deficit, stomata number and size, photosynthetic and respiration rate in the area of the tobacco leaf blade. Biol Plantarum 5:143–53.
Smith H (1970). Changes in plastid ribosomal-RNA and enzymes during the growth of barley leaves in darkness. Phytochemistry 9:965–75.
Smith JAC, Heuer S (1981). Determination of the volume of intercellular spaces in leaves and some values for CAM plants. Ann Bot-London 48:915–7.
Soper K, Mitchell K (1956). The developmental anatomy of perennial ryegrass (Lolium perenne L.) New Zeal J Sci 37:484–504.
Steer MW (1981). Understanding cell structure. Cambridge University Press, Cambridge.
Sterio D (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc-Oxford 134:127–36.
Stettler M, Eicke S, Mettler T, Messerli G, Hörtensteiner S, Zeeman SC (2009). Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2:1233–46.
Sung F, Chen J (1989). Changes in photosynthesis and other chloroplast traits in lanceolate leaflet isoline of soybean. Plant Physiol 90:773–7.
Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006). Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103.
Thain J (1983). Curvature Correction Factors in the Measurement of Cell Surface Areas in Plant Tissues 1. J Exp Bot 34:87–94.
Théroux-Rancourt G, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, McElrone AJ, Brodersen CR (2017). The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging. New Phytol 215:1609–22.
Tichá I, Čatský J (1977). Ontogenetic changes in the internal limitations to bean leaf photosynthesis, 3: Leaf mesophyll structure and intracellular conductance for carbon dioxide transfer. Photosynthetica 11:361-6.
Turrell FM (1934). Leaf surface of a twenty-one-year old catalpa tree. Proc Iowa Acad Sci 41:79–84.
Turrell FM (1936). The area of the internal exposed surface of dicotyledon leaves. Am J Bot 23:255–64.
Tymms MJ, Scott NS, Possingham JV (1983). DNA content of Beta vulgaris chloroplasts during leaf cell expansion. Plant Physiol 71:785–8.
Unger F (1854). Beiträge zur Physiologie der Pflanzen. Sitzber d Wien Akad d Wiss 12:367.
Vassilyev AE (2000). Quantitative ultrastructural data of secretory duct epithelial cells in Rhus toxicodendron. Int J Plant Sci 161:615–30.
Vičánková A, Kutík J (2005). Chloroplast ultrastructural development in vascular bundle sheath cells of two different maize (Zea mays L.) genotypes. Plant Soil Environ 51:491–5.
Wang X, Anderson OR, Griffin KL (2004). Chloroplast numbers, mitochondrion numbers and carbon assimilation physiology of Nicotiana sylvestris as affected by CO2 concentration. Environ Exp Bot 51:21–31.
Wehrmeyer W, Röbbelen G (1965). Räumliche Aspekte zur Membranschichtung in den Chloroplasten einer Arabidopsis-Mutante unter Auswertung von Serienschnitten. Planta 64:312–29.
Weibel ER (1979). Stereological methods, Vol 1. Practical methods for biological morphometry. Academic Press, London.
Wheeler W, Fagerberg W (2000). Exposure to low levels of photosynthetically active radiation induces rapid increases in palisade cell chloroplast volume and thylakoid surface area in sunflower (Helianthus annuus L.) Protoplasma 212:38–45.
Wild A, Wolf G (1980). The effect of different light intensities on the frequency and size of stomata, the size of cells, the number, size and chlorophyll content of chloroplasts in the mesophyll and the guard cells during the ontogeny of primary leaves of Sinapis alba. Z Pflanzenphysiol 97:325–42.
Wilson D, Cooper J (1967). Assimilation of Lolium in relation to leaf mesophyll. Nature 214:989–92.
Wulff A, Ahonen J, Kärenlampi L (1996). Cell ultrastructural evidence of accelerated ageing of Norway spruce needles in industrial areas. New Phytol 133:553–61.
Wylie RB (1949). Differences in foliar organization among leaves from four stations in the crown of an isolated tree (Acer platanoides). Proc Iowa Acad Sci 56:189–98.
Xu C-Y, Salih A, Ghannoum O, Tissue DT (2012). Leaf structural characteristics are less important than leaf chemical properties in determining the response of leaf mass per area and photosynthesis of Eucalyptus saligna to industrial-age changes in [CO2] and temperature. J Exp Bot 63:5829–41.
Yamasaki T, Kudoh T, Kamimura Y, Katoh S (1996). A vertical gradient of the chloroplast abundance among leaves of Chenopodium album. Plant Cell Physiol 37:43–8.
Yiotis C, Psaras GK (2011). Dianthus caryophyllus stems and Zantedeschia aethiopica petioles/pedicels show anatomical features indicating efficient photosynthesis. Flora-Morphology, Distribution, Functional Ecology of Plants 206:360–4.
Yu W, Liu Y, Song L, Jacobs DF, Du X, Ying Y, Shao Q, Wu J (2017). Effect of differential light quality on morphology, photosynthesis, and antioxidant enzyme activity in Camptotheca acuminata seedlings. J Plant Growth Regul 36:148–160.
Zechmann B, Müller M, Zellnig G (2003). Cytological modifications in zucchini yellow mosaic virus (ZYMV)-infected Styrian pumpkin plants. Arch Virol 148:1119–33.
Zellnig G, Zechmann B, Perktold A (2004). Morphological and quantitative data of plastids and mitochondria within drought-stressed spinach leaves. Protoplasma 223:221–7.
Zorić L, Luković J, Matić-Kekić S, Merkulov L (2011). Modified stereological method for analysis of compound leaves and an example of its application. J Biol Syst 19:617–27.
Zorić L, Mikić A, Ćupina B, Luković J, Krstić D, Antanasović S (2014). Digestibility-related histological attributes of vegetative organs of barrel medic (Medicago truncatula Gaertn.) cultivars 3:257–64.
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