Coping with spring frost-effects on polyamine metabolism of Scots pine seedlings

doi:10.3832/ifor2003-009

Coping with spring frost-effects on polyamine metabolism of Scots pine seedlings

Riina Muilu-Mäkelä^(1-2) , Jaana Vuosku⁽²⁾, Markku Saarinen⁽¹⁾, Leena Hamberg⁽³⁾, Seppo Ruotsalainen⁽⁴⁾, Hely Häggman⁽²⁾, Tytti Sarjala⁽¹⁾

iForest - Biogeosciences and Forestry, Volume 10, Issue 1, Pages 227-236 (2017)
doi: https://doi.org/10.3832/ifor2003-009
Published: Jan 27, 2017 - Copyright © 2017 SISEF

Research Articles

PDF Version

Full Text

Citation

Geo-mapping

Polyamines (PA) are ubiquitous polycations known to be involved in several phases of plant development as well as in tolerance to abiotic stresses. Phenols are complex secondary metabolites produced via the phenylpropanoid pathway that contain, e.g., cell wall compounds and antioxidants. Phenols are known to enhance chilling tolerance of plants. PA and phenolic pathways are connected via conjugation. In boreal coniferous forests spring frost has been considered to have severe effects on the survival of tree seedlings. Such effects are likely to increase in the future. The present study focuses on the role of PA and phenylpropanoid syntheses in the coping strategies of Scots pine exposed to cold temperatures during the vulnerable early seedling phase in late spring and early summer. We found that spring frost affects the expression of genes regulating PA metabolism and phenylpropanoid synthesis differently in above and below ground parts of the seedlings, whereas PA or phenol contents in tissues were not affected. The results suggest that Scots pine seedlings may not have time to develop metabolite level responses during a short period of freezing stress and, therefore, the originally different PA levels, especially in roots, may influence the tolerance of Scots pine seedlings to spring frost.

Keywords

Phenylpropanoids, Polyamines, Scots Pine, Spring Frost

Authors’ address

(1)

Natural Resources Institute Finland (Luke), Parkano Research Unit, FI-39700 Parkano (Finland)

(2)

Genetics and Physiology department, University of Oulu, P.O. Box 3000, FI-90014 Oulu (Finland)

(3)

Natural Resources Institute Finland (Luke), Vantaa Research Unit, FI- 01370, Vantaa (Finland)

(4)

Natural Resources Institute Finland (Luke), Punkaharju Research Unit, FI-58450, Punkaharju (Finland)

Corresponding author

Riina Muilu-Mäkelä
riina.muilu-makela@luke.fi

Citation

Muilu-Mäkelä R, Vuosku J, Saarinen M, Hamberg L, Ruotsalainen S, Häggman H, Sarjala T (2017). Coping with spring frost-effects on polyamine metabolism of Scots pine seedlings. iForest 10: 227-236. - doi: 10.3832/ifor2003-009

Academic Editor

Mike Perks

Paper history

Received: Feb 05, 2016
Accepted: Nov 27, 2016

First online: Jan 27, 2017
Publication Date: Feb 28, 2017
Publication Time: 2.03 months

Open Access

This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 39722
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 33785
Abstract Page Views: 1879
PDF Downloads: 3047
Citation/Reference Downloads: 35
XML Downloads: 976

Web Metrics
Days since publication: 2640
Overall contacts: 39722
Avg. contacts per week: 105.32

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2017): 3
Average cites per year: 0.43

(no Plumx Metrics available for this paper)

Publication Metrics

by Dimensions ^©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

(1)

Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011)
Integration of polyamines in the cold acclimation response. Plant Science 180: 31-38.
CrossRef | Gscholar

(2)

Bassard JE, Ullmann P, Bernier F, Werck-Reichhart D (2010)
Phenolamides: bridging polyamines to phenolic metabolism. Phytochemistry 71: 1808-1824.
CrossRef | Gscholar

(3)

Beck EH, Heim R, Hansen J (2004)
Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. Journal of Bioscience 29: 449-459.
CrossRef | Gscholar

(4)

Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke J, Blais S, Tremblay L, Morency M-J, Pavy N, Grima-Pettenati J, Séguin A, MacKay J (2014)
Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. Journal of Experimental Botany 59: 3925-3939.
CrossRef | Gscholar

(5)

Boudet AM (2007)
Evolution and current status of research in phenolic compounds. Phytochemistry 68: 2722-2735.
CrossRef | Gscholar

(6)

Chinnusamy V, Zhu J, Zhu J-K (2007)
Cold stress regulation of gene expression in plants. Trends in Plant Science 12: 444-451.
CrossRef | Gscholar

(7)

Chong J, Poutaraud A, Hugueney P (2009)
Metabolism and roles of stilbenes in plants. Plant Science 177: 143-155.
CrossRef | Gscholar

(8)

Craven-Bartle B, Pascual MB, Cánovas FM, Avila C (2013)
A Myb transcription factor regulates genes of the phenylalanine pathway in maritime pine. The Plant Journal 74: 755-766.
CrossRef | Gscholar

(9)

Douglas CJ (1996)
Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends in Plant Science 1: 171-178.
CrossRef | Gscholar

(10)

Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010)
MYB transcription factors in Arabidopsis. Trends in Plant Science 15: 573-581.
CrossRef | Gscholar

(11)

Fornalé S, Sarjala T, Bagni N (1999)
Endogenous polyamine content and metabolism in the ectomycorrhizal fungus Paxillus involutus. New Phytologist 143: 581-587.
CrossRef | Gscholar

(12)

Gaquerel E, Gulati J, Baldwin IT (2014)
Revealing insect herbivory-induced phenolamide metabolism: from single genes to metabolic network plasticity analysis. Plant Journal 79: 679-692.
CrossRef | Gscholar

(13)

Groppa MD, Benavides MP (2008)
Polyamines and abiotic stress: recent advances. Amino Acids 34 (1): 35-45.
CrossRef | Gscholar

(14)

Guo Z, Tan J, Zhuo C, Wang C, Xiang B, Wang Z (2014)
Abscisic acid, H₂O₂ and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. Falcate that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnology Journal 12: 601-612.
CrossRef | Gscholar

(15)

Häggman H, Pirttilä AM, Niemi K, Sarjala T, Julkunen-Tiitto R (2009)
Medicinal properties, In vitro protocols and secondary metabolite analyses of Scots pine. Methods of Molecular Biology 547: 35-52.
CrossRef | Gscholar

(16)

Hänninen H (2006)
Climate warming and the risk of frost damage to boreal forest trees: identification of critical ecophysiological traits. Tree Physiology 26: 889-898.
CrossRef | Gscholar

(17)

Hatmi S, Trotel-Aziz P, Villaume S, Couderchet M, Clément C, Aziz A (2014)
Osmotic stress-induced polyamine oxidation mediates defence responses and reduces stress-enhanced grapevine susceptibility to Botrytis cinerea. Journal of Experimental Botany 65: 75-88.
CrossRef | Gscholar

(18)

Jensen KM, Cvikrová M, Paltgiewicz A, Eder J (2000)
Alterations in phenylpropanoid content in soybean roots during low temperature acclimation. Plant Physiology and Biochemistry 38: 587-593.
CrossRef | Gscholar

(19)

Johnsen O, Fossdal CG, Nagy N, Skroppa T (2005)
Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant Cell Environment 28: 1090-1102.
CrossRef | Gscholar

(20)

Joosen R, Lammers M, Balk PA, Bronnum P, Konings M, Perks M, Stattin E, Wordragen M, Van Der Geest A (2005)
Correlating gene expression to physiological parameters and environmental conditions during cold acclimation of Pinus sylvestris, identification of molecular markers using cDNA microarrays. Tree Physiology 26: 1297-1313.
CrossRef | Gscholar

(21)

Juntunen V, Neuvonen S (2006)
Natural regeneration of Scots pine and Norway spruce close to the timberline in northern Finland. Silva Fennica 40: 443-458.
CrossRef | Gscholar

(22)

Koag M-C, Wilkens S, Fenton RD, Resnik J, Vo E, Close TJ (2009)
The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. American Society of Plant Biology 150: 1503-1514.
Online | Gscholar

(23)

Kontunen-Soppela S, Taulavuori K, Taulavuori E, Lähdesmäki P, Laine K (2000)
Soluble proteins and dehydrins in nitrogen-fertilized Scots pine seedlings during deacclimation and the onset of growth. Physiologia Plantarum 109: 404-409.
CrossRef | Gscholar

(24)

Krasensky J, Jonak C (2012)
Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63: 1593-1608.
CrossRef | Gscholar

(25)

Kujala S, Savolainen O (2012)
Sequence variation patterns along a latitudinal cline in Scots pine (Pinus sylvestris): signs of clinal adaptation? Tree Genetics and Genome 8: 1451-1467.
CrossRef | Gscholar

(26)

Langwall O (2011)
Impact of climate change, seedling type and provenance on the risk of damage to Norway spruce (Picea abies (L.) Karst.) seedlings in Sweden due to early summer frosts. Scandinavian Journal of Forest Research 26: 56-63.
CrossRef | Gscholar

(27)

Leinonen I, Repo T, Hänninen H (1997)
Changing environmental effects on frost hardiness of Scots pine during dehardening. Annals of Botany 79: 133-138.
CrossRef | Gscholar

(28)

Linkosalo T (2000)
Analyses of the spring phenology of boreal trees and its response to climate change. University of Helsinki, Department of Forest Ecology Publications 22, Helsingin yliopiston verkkojulkaisut, Helsinki, Finland, pp. 55.
Gscholar

(29)

Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008)
Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Science 174: 420-431.
CrossRef | Gscholar

(30)

Muilu-Mäkelä R, Vuosku J, Läärä E, Häggman H, Saarinen M, Heiskanen J, Sarjala T (2015a)
Water availability influence morphology, mycorrhizal associations, PSII efficiency and polyamine metabolism at early growth phase of Scots pine seedlings. Plant Physiology and Biochemistry 88: 70-81.
CrossRef | Gscholar

(31)

Muilu-Mäkelä R, Vuosku J, Hamberg L, Latva-Mäenpää H, Häggman H, Sarjala T (2015b)
Osmotic stress affects polyamine homeostasis and phenolic content in proembryogenic liquid cell cultures of Scots pine. Plant Cell, Tissue and Organ Culture 122: 709-726.
CrossRef | Gscholar

(32)

Nygren M (2011)
Metsänkylvöopas - Kylvön biologiaa ja tekniikkaa [Forest sowing book - biology and techniques of sowing]. Metsäntutkimuslaitos, Vantaa, 85 s. [in Finnish]
Gscholar

(33)

Pinheiro J, Bates D, DebRoy S, Sarkar D, Core RT (2014)
nlme: linear and nonlinear mixed effects models. R package version 3: 1-117.
Online | Gscholar

(34)

Pottosin I, Velarde-Buendía AM, Bose J, Zapenda-Jazo I, Shabala S, Dobrovinskaya O (2014)
Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. Journal of Experimental Botany 65: 1271-1283.
CrossRef | Gscholar

(35)

R Core Team (2014)
R: a language and environment for statistical computing. R Foundation for Statistical Computing, Wien, Austria.
Online | Gscholar

(36)

Rikala R, Repo T (1987)
Frost resistance and frost damage in Pinus sylvestris seedlings during shoot elongation. Scandinavian Journal of Forest Research 2: 433-440.
CrossRef | Gscholar

(37)

Ryyppö A, Iivonen S, Rikala R, Sutinen M-L, Vapaavuori E (1998)
Response of Scots pine seedlings to low temperature in spring. Physiologia Plantarum 102: 503-512.
CrossRef | Gscholar

(38)

Saarinen M (2013)
Männyn kylvö ja luontainen taimettuminen vanhoilla ojitusalueilla - turvemaiden uudistamisen erityispiirteitä [Artificial and natural seeding of Scots pine in old drainage areas - Unique features of forest regeneration on peat lands]. Dissertationes Forestales 164, University of Helsinki, Finnish Society of Forest Science, Helsinki, Finland, pp. 64. [in Finnish]
Gscholar

(39)

Sarjala T, Kaunisto S (1993)
Needle polyamine concentrations and potassium nutrition in Scots pine. Tree Physiology 13: 87-96.
CrossRef | Gscholar

(40)

Shi Y, Ding Y, Yang S (2015)
Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiology 56: 7-15.
CrossRef | Gscholar

(41)

Singleton VL, Orthofer R, Lamuela-Raventos RM (1999)
Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 299: 152-178.
CrossRef | Gscholar

(42)

Solecka D, Kacperska A (2003)
Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiologia Plantarum 119: 253-262.
CrossRef | Gscholar

(43)

Tang W, Newton RJ, Li C, Charles TM (2007)
Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Reports 26: 115-124.
CrossRef | Gscholar

(44)

Tang W, Newton RJ (2005)
Polyamines promote root elongation and growth by increasing root cell division in regenerated Virginia pine (Pinus virginiana Mill.) plantlets. Plant Cell Reports 24: 581-589.
CrossRef | Gscholar

(45)

Theocharis A, Clément C, Barka EA (2012)
Physiological and molecular changes in plants grown at low temperatures. Planta 235: 1091-1105.
CrossRef | Gscholar

(46)

Vapaavuori EM, Rikala R, Ryyppö A (1992)
Effect of root temperature on growth and photosynthesis in conifer seedlings during shoot elongation. Tree Physiology 10: 217-230.
CrossRef | Gscholar

(47)

Viitala K, Potila H, Savonen E-M, Sarjala T (2011)
Health from forest - Antioxidative properties of endophytic fungi from Scots pine roots. In: Proceedings of the 7th International Conference on “Mushroom Biology and Mushroom Products - ICMBMP7” (Savoie J-M, Foulongne-Oriol M, Largeteau M, Barroso G eds). Arcachon (France) 4-7 Oct 2011. INRA, UR1264, Mycology and Food Safety, Bordeaux, France, vol. 2, pp. 103-109.
Gscholar

(48)

Vuosku J, Sutela S, Kestilä J, Jokela A, Sarjala T, Häggman H (2015)
Expression of catalase and retinoblastoma-related protein genes associated with cell death processes in Scots pine zygotic embryogenesis. BMC Plant Biology 15: 88.
CrossRef | Gscholar

(49)

Yakovlev I, Asante D, Fossdal C, Junttila O, Johnsen O (2011)
Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Science 180: 132-139.
CrossRef | Gscholar

(50)

Yang Y, He M, Zhu Z, Li S, Xu Y, Zhang C, Singer SD, Wang Y (2012)
Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness to various forms of abiotic and biotic stress. BMC Plant Biology 12 (1): 140.
CrossRef | Gscholar

iForest - Biogeosciences and Forestry

Contents

Search

Journal Info

Journal Subjects and Fields

For Authors

For Reviewers

For Readers

SISEF Publishing

Search iForest Contents