Abstract
Control of freezing in plant tissues is a key issue in cold hardiness mechanisms. Yet freeze-regulation mechanisms remain mostly unexplored. Among them, ice nucleation activity (INA) is a primary factor involved in the initiation and regulation of freezing events in plant tissues, yet the details remain poorly understood. To address this, we developed a highly reproducible assay for determining plant tissue INA and noninvasive freeze visualization tools using MRI and infrared thermography. The results of visualization studies on plant freezing behaviors and INA survey of over 600 species tissues show that (1) freezing-sensitive plants tend to have low INA in their tissues (thus tend to transiently supercool), while wintering cold-hardy species have high INA in some specialized tissues; and (2) the high INA in cold-hardy tissues likely functions as a freezing sensor to initiate freezing at warm subzero temperatures at appropriate locations and timing, resulting in the induction of tissue-/species-specific freezing behaviors (e.g., extracellular freezing, extraorgan freezing) and the freezing order among tissues: from the primary freeze to the last tissue remaining unfrozen (likely INA level dependent). The spatiotemporal distributions of tissue INA, their characterization, and functional roles are detailed. INA assay principles, anti-nucleation activity (ANA), and freeze visualization tools are also described.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
Abbreviations
- ANA:
-
Anti-nucleation activity
- DTA:
-
Differential thermal analysis
- INA:
-
Ice nucleation activity
- INT:
-
Ice nucleation temperature
- IR:
-
Infrared
- MRI:
-
Magnetic resonance imaging
- SEM:
-
Scanning electron microscopy
References
Ashworth EN, Davis GA (1984) Ice nucleation within peach trees. J Amer Soc Hort Sci 109:198–201
Ashworth EN, Kieft TL (1995) Ice nucleation activity associated with plants and fungi. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 137–162
Ball MC, Wolfe J, Canny M, Hofmann M, Nicotra AB, Hughes D (2002) Space and time dependence of temperature and freezing in evergreen leaves. Func Plant Biol 29:1259–1272
Borisjuk L, Rolletschek H, Neuberger T (2012) Surveying the plant’s world by magnetic resonance imaging. Plant J 70:129–146
Brush RA, Griffith M, Mlynarz A (1994) Characterization and quantification of intrinsic ice nucleators in winter rye (Secale cereale) leaves. Plant Physiol 104:725–735
Callaghan PT (1991) Principles of nuclear magnetic resonance microscopy. Oxford University Press, Oxford
Dean RJ, Stait-Gardner T, Clarke SJ, Rogiers SY, Bobek G, Price WS (2014) Use of diffusion magnetic resonance imaging to correlate the developmental changes in grape berry tissue structure with water diffusion patterns. Plant Methods 10:35–48
Fall R, Wolber PK (1995) Biochemistry of bacterial ice nuclei. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 63–83
Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390
Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge
Fukuda K, Kawaguchi D, Aihara T, Ogasa MY, Miki NH, Haishi T, Umebayashi T (2015) Vulnerability to cavitation differs between current-year and older xylem: non-destructive observation with a compact magnetic resonance imaging system of two deciduous diffuse-porous species. Plant Cell Environ 38:2508–2518
Gross DC, Proebsting EL Jr, Maccrindle-Zimmerman H (1988) Development, distribution, and characteristics of intrinsic, nonbacterial ice nuclei in Prunus wood. Plant Physiol 88:915–922
Gupta A, Stait-Gardner T, Ghadirian B, Price WS (2014) Fundamental concepts for the theory, dynamics of MRI. In: Awojoyogbe OB (ed) Theory, dynamics and applications of magnetic resonance imaging-I. Science Publishing Group, New York, pp 3–37
Hacker J, Neuner G (2008) Ice propagation in dehardened alpine plant species studied by infrared differential thermal analysis (IDTA). Arc Antarc Alpine Res 40:660–670
Hirano SS, Upper CD (1995) Ecology of ice nucleation-active bacteria. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 41–61
Hirano SS, Baker LS, Upper CD (1985) Ice nucleation temperature of individual leaves in relation to population sizes of ice nucleation active bacteria and frost injury. Plant Physiol 77:259–265
Ide H, Price WS, Arata Y, Ishikawa M (1998) Freezing behaviors in leaf buds of cold-hardy conifers visualized by NMR microscopy. Tree Physiol 18:451–458
Ishikawa M (2014) Ice nucleation activity in plant tissues. Cryobiol Cryotech 60:79–88
Ishikawa M (2016) Factors contributing to freeze regulation in cold hardy plant tissues. In: Abstracts of 61st seminar for cryobiology and cryotechnology, Tokyo Denki University, Hatoyama, 25–26 June 2016
Ishikawa M, Sakai A (1981) Freezing avoidance mechanisms by supercooling in some Rhododendron flower buds with reference to water relations. Plant Cell Physiol 22:953–967
Ishikawa M, Sakai A (1985) Extraorgan freezing in wintering flower buds of Cornus officinalis Sieb. et Zucc. Plant Cell Environ 8:333–338
Ishikawa M, Price WS, Ide H, Arata Y (1997) Visualization of freezing behaviors in leaf and flower buds of full-moon maple by nuclear magnetic resonance microscopy. Plant Physiol 115:1515–1524
Ishikawa M, Ide H, Price WS, Arata Y, Nakamura T, Kishimoto T (2009) Freezing behaviours in plant tissues: visualization using NMR micro-imaging and biochemical regulatory factors involved. In: Gusta LV, Tanino KK, Wisniewski ME (eds) Plant cold hardiness: from the laboratory to the field. CABI, Cambridge, pp 19–28
Ishikawa M, Ishikawa M, Toyomasu T, Aoki T, Price WS (2015) Ice nucleation activity in various tissues of Rhododendron flower buds: their relevance to extraorgan freezing. Front Plant Sci 6:149
Ishikawa M, Ide H, Yamazaki H, Murakawa H, Kuchitsu K, Price WS, Arata Y (2016) Freezing behaviors in wintering Cornus florida flower bud tissues revisited using MRI. Plant Cell Environ 39:2663–2675
Ishikawa M, Ide H, Tsujii T, Kuchitsu K, Price WS, Arata Y (2018) Preferential freezing avoidance localized in anthers and embryo sacs in wintering Daphne kamtschatica var. jezoensis flower buds visualized by MRI. Plant Cell Environ (accepted)
Kasuga J, Hashidoko Y, Nishioka A, Yoshiba M, Arakawa K, Fujikawa S (2008) Deep supercooling xylem parenchyma cells of katsura tree (Cercidiphyllum japonicum) contain flavonol glycosides exhibiting high anti-ice nucleation activity. Plant Cell Environ 31:1335–1348
Kishimoto T, Sekozawa Y, Yamazaki H, Murakawa H, Kuchitsu K, Ishikawa M (2014a) Seasonal changes in ice nucleation activity in blueberry stems and effects of cold treatments in vitro. Environ Exp Bot 106:13–23
Kishimoto T, Yamazaki H, Saruwatari A, Murakawa H, Sekozawa Y, Kuchitsu K, Price WS, Ishikawa M (2014b) High ice nucleation activity located in blueberry stem bark is linked to primary freeze initiation and adaptive freezing behavior of the bark. AoB Plants 6:plu044
Kitaura K (1967) Freezing and injury of mulberry trees by late spring frost. Bull Seric Exp Station 22:202–323
Köckenberger W (2001) Functional imaging of plants by magnetic resonance experiments. Trends in Plant Sci 6:286–292
Kuprian E, Briceno V, Wagner J, Neuner G (2014) Ice barriers promote supercooling and prevent frost injury in reproductive buds, flowers and fruits of alpine dwarf shrubs throughout the summer. Environ Exp Bot 106:4–12
Kuroda H, Sagisaka S, Chiba K (1990) Frost induces cold acclimation and peroxide scavenging systems coupled with the pentose phosphate cycle in apple twigs under natural conditions. J Jpn Soc Hort Sci 59:409–416
Larcher W, Meindl U, Ralser E, Ishikawa M (1991) Persistent supercooling and silica deposition in cell walls of palm leaves. J Plant Physiol 139:146–154
Lindow SE (1983) The role of bacterial ice nucleation in frost injury to plants. Annu Rev Phytopathol 21:363–384
Nagata A, Kose K, Terada Y (2016) Development of an outdoor MRI system for measuring flow in a living tree. J Magn Reson 265:129–138
Neuner G (2014) Frost resistance in alpine woody plants. Front Plant Sci 5:1–13
Neuner G, Xu B, Hacker J (2010) Velocity and pattern of ice propagation and deep supercooling in woody stems of Castanea sativa, Morus nigra and Quercus robur measured by IDTA. Tree Physiol 30:1037–1045
Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424
Price WS, Ide H, Arata Y, Ishikawa M (1997a) Visualization of freezing behaviours in flower bud tissues of cold hardy Rhododendron japonicum by nuclear magnetic resonance micro-imaging. Aust J Plant Physiol 24:599–605
Price WS, Ide H, Ishikawa M, Arata Y (1997b) Intensity changes in 1H-NMR micro-images of plant materials exposed to subfreezing temperatures. Bioimages 5:91–99
Pruppacher HR (1967) Interpretation of experimentally determined growth rates of ice crystals in supercooled water. J Chem Phys 47:1807–1813
Quamme HA (1995) Deep supercooling in buds of woody plants. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 183–200
Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress, ecological studies 62. Springer-Verlag, Berlin
Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–239
Sekozawa Y, Sugaya S, Gemma H, Iwahori S, Ishikawa M (2002) Seasonal changes in the ice nucleation activity of various tissues in Japanese pear (Pyrus pyrifolia Nakai) in relation to their freezing behavior and frost injury. Acta Hort 587:543–547
Thomashow MF (1999) Plant cold acclimation, freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 50:571–599
Tsushima K (2015) Ice and snow physics (online textbook). http://profeme.u-toyama.ac.jp/Tusima_Books/Ice_and_Snow_physics_2015_ver_08.pdf. Accessed 15 Sept 2017
Ueda Y, Anma K, Ishikawa M (2002) Variation of Rosa and its genealogical implication in cultivated roses. 9. Ice nucleating activity of Rosa species. Proc Jpn Soc Hort Sci 71(suppl 1):293
Upper CD, Vali G (1995) The discovery of bacterial ice nucleation and its role in the injury of plants by frosts. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 29–39
Vali G (1971) Quantitative evaluation of experimental results on the heterogeneous freezing nucleation of supercooled liquids. J Atmos Sci 28:402–409
Vali G (1995) Principles of ice nucleation. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 1–28
Vali G, Stansbury EJ (1966) Time-dependent characteristics of the heterogeneous nucleation of ice. Can J Phys 44:477–502
Venturas MD, Sperry JS, Hacke UG (2017) Plant xylem hydraulics: what we understand, current research, and future challenges. J Integ Plant Biol 59:356–389
Warren GJ (1995) Identification and analysis of ina genes and proteins. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 85–99
Wisniewski M, Lindow SE, Ashworth EN (1997) Observations of ice nucleation and propagation in plants using infrared video thermography. Plant Physiol 113:327–334
Wisniewski ME, Gusta LV, Fuller MP, Karlson D (2009) Ice nucleation, propagation and deep supercooling: the lost tribes of freezing studies. In: Gusta LV, Tanino KK, Wisniewski ME (eds) Plant cold hardiness: from the laboratory to the field. CABI, Cambridge, pp 1–11
Yamazaki H, Ishikawa M (2010) Analysis of freezing behavior in blueberry stems visualized using differential infra-red thermography. Cryobiol Cryotech 56:91–95
Yamazaki H, Yoshida S, Ishikawa M (2011) Freezing behavior in blueberry stems analyzed using differential infra-red thermography and differential thermal analysis. Cryobiol Cryotech 57:77–81
Acknowledgments
The authors thank Ms. Kitashima, Kitanaka, Oda, Nakatani, and Ishikawa of NIAS for their technical assistance. The authors acknowledge the facilities and the scientific and technical assistance of the National Imaging Facility, Western Sydney University Node. This was partly supported by JSPS KAKENHI Grant numbers JP17H03763, JP26660030, JP23380023, and JP16380030 to M.I., IBBP Research Fund from Japan Society for the Promotion of Science to M.I., the New Technology Development Foundation (Plant Research Fund 25–23, 26-22) and Kieikai Research Foundation (2016S069) to K.K.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Ishikawa, M. et al. (2018). Ice Nucleation Activity in Plants: The Distribution, Characterization, and Their Roles in Cold Hardiness Mechanisms. In: Iwaya-Inoue, M., Sakurai, M., Uemura, M. (eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology, vol 1081. Springer, Singapore. https://doi.org/10.1007/978-981-13-1244-1_6
Download citation
DOI: https://doi.org/10.1007/978-981-13-1244-1_6
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-1243-4
Online ISBN: 978-981-13-1244-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)