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Engineering Polyamine Metabolic Pathways for Abiotic Stress Tolerance in Plants

  • Susana de Sousa Araújo
  • André Luis Wendt dos Santos
  • Ana Sofia DuqueEmail author
Chapter

Abstract

In the current scenario of climate change, plants are being challenged with frequent episodes of extreme weather events and suffer recurrently from various abiotic stresses that negatively affect growth and development and limit plant productivity. Abiotic stresses activate the expression of several stress-related genes, leading to the synthesis of active proteins and accumulation of metabolites, and other osmotically active compounds. Among these compounds, we can highlight the polyamines (PAs), interesting biomolecules that play an important role on plant physiology, development, and response to environment. PAs are low-molecular-weight, positively charged, aliphatic amines that are found widespread in living organisms. In plants, the most abundant PAs are putrescine (Put), spermidine (Spd), and spermine (Spm). They are synthesized from decarboxylation of amino acids, mainly arginine and ornithine. Put is synthesized primarily through the activity of the enzymes arginine decarboxylase (ADC) and ornithine decarboxylase (ODC). Put is then converted into Spd by spermidine synthase (SPDS), and Spd is further converted into Spm by Spm synthase (SPMS). PA levels in plants increase under a number of environmental stress conditions, including drought, high salinity, and exposure to extreme temperatures (heating or freezing). Numerous studies have provided evidences that enhanced accumulation of PAs in plants is correlated with increased resistance to adverse environmental conditions. In this chapter, we will provide a current state of the art on the works related to the development of plants with altered PA contents, by the manipulation of PA metabolic pathways through genetic engineering, and discussed the possible associated effects on several abiotic stresses.

Keywords

Abiotic stress Tolerance Drought Salinity Extreme temperatures Transgenic plants Manipulation polyamine metabolism 

Notes

Acknowledgments

Financial support from FCT (Fundação para a Ciência e Tecnologia, Lisbon, Portugal) is acknowledged through the research unit “GREEN-it: Bioresources for Sustainability” (UID/Multi/04551/2013) and through ASD and SSA PhD holders DL57 research contracts. ALWS is supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) and Young Investigators Grants 15/21075-4 and 17/01284-3. ALWS thanks Dra. Eny IS Floh (Department of Botany, University of São Paulo) for her valuable collaboration and pioneering studies with polyamines in Brazil.

References

  1. Alcázar R, García-Martínez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J 43:425–436.  https://doi.org/10.1111/j.1365-313X.2005.02465.xCrossRefPubMedPubMedCentralGoogle Scholar
  2. Alcázar R, Cuevas JC, Patron M, Altabella T, Tiburcio AF (2006) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455CrossRefGoogle Scholar
  3. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010a) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefPubMedCentralGoogle Scholar
  4. Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas JC, Bitrián M, Tiburcio AF, Altabella T (2010b) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous Arginine decarboxylase 2 gene. Plant Physiol Biochem 48(7):547–552PubMedCrossRefPubMedCentralGoogle Scholar
  5. Alet AI, Sanchez DH, Cuevas JC, del Valle S, Altabella T, Tiburcio AF, Marco F, Ferrando A, Espasandín FD, González ME, Carrasco P, Ruiz OA (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286.  https://doi.org/10.4161/psb.6.2.14702CrossRefPubMedPubMedCentralGoogle Scholar
  6. Altabella T, Tiburcio AF, Ferrando A (2009) Plant with resistance to low temperature and method of production thereof. Spanish patent application; WO2010/004070; US patent application; No:2011/0126,322Google Scholar
  7. Anwar A, She M, Wang K, Riaz B, Ye X (2018) Biological roles of ornithine aminotransferase (OAT) in plant stress tolerance: present progress and future perspectives. Int J Mol Sci 19:3681.  https://doi.org/10.3390/ijms19113681CrossRefGoogle Scholar
  8. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J Plant Growth Regul 28:177–186.  https://doi.org/10.1007/s00344-009-9086-7CrossRefGoogle Scholar
  9. Araújo SS, Beebe S, Crespi M, Delbreil B, González EM, Gruber V, Lejeune-Henaut I, Link W, Monteros MJ, Prats E, Rao I, Vadez V, Vaz Patto MC (2015) Abiotic stress responses in Legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280.  https://doi.org/10.1080/07352689.2014.898450CrossRefGoogle Scholar
  10. Asseng S, Foster I, Turner NC (2011) The impact of temperature variability on wheat yields. Glob Chang Biol 17:997–1012.  https://doi.org/10.1111/j.1365-2486.2010.02262.xCrossRefGoogle Scholar
  11. Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44:384–395.  https://doi.org/10.1007/s11627-008-9176-4CrossRefGoogle Scholar
  12. Bastola DR, Minocha SC (1995) Increased putrescine biosynthesis through transfer of mouse ornithine decarboxylase cDNA in carrot promotes somatic embryogenesis. Plant Physiol 109:63–71PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bokszczanin K, Fragkostefanakis S, Bostan H, Bovy A, Chaturvedi P, Chiusano M, Firon N, Iannacone R, Jegadeesan S, Klaczynskid K, Li H, Mariani C, Müller F, Paul P, Paupiere M, Pressman E, Rieu I, Scharf K, Schleiff E, Van Heusden A, Vriezen W, Weckwerth W, Winter P (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 4:315.  https://doi.org/10.3389/fpls.2013.00315CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bor M, Özdemir F (2018) Manipulating metabolic pathways for development of salt-tolerant crops. In: Kumar V, Wani S, Suprasanna P, Tran LS (eds) Salinity responses and tolerance in plants, vol 1. Springer International Publishing, Cham, pp 235–256CrossRefGoogle Scholar
  15. Borrell A, Besford RT, Altabella T, Masgrau C, Tiburcio AF (1996) Regulation of arginine decarboxylase by spermine in osmotically-stressed oat leaves. Physiol Plant 98:105–110CrossRefGoogle Scholar
  16. Bouchereau A, Guénot P, Larher F (2000) Analysis of amines in plant materials. J Chromatogr B 747:49–67CrossRefGoogle Scholar
  17. Burtin D, Michael AJ (1997) Over-expression of arginine decarboxylase in transgenic plants. Biochem J 325:331–337PubMedPubMedCentralCrossRefGoogle Scholar
  18. Capell T, Escobar C, Liu H, Burtin D, Lepri O, Christou P (1998) Overexpression of the oat arginine decarboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor Appl Genet 97:246–254CrossRefGoogle Scholar
  19. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci U S A 101(26):9909–9914PubMedPubMedCentralCrossRefGoogle Scholar
  20. Champa WAH, Gill MIS, Mahajan BVC, Bedi S (2015) Exogenous treatment of spermine to maintain quality and extend postharvest life of table grapes (Vitis vinifera L.) cv. Flame Seedless under low temperature storage. LWT – Food Sci Technol 60:412–419.  https://doi.org/10.1016/j.lwt.2014.08.044CrossRefGoogle Scholar
  21. Channarayappa C, Biradar DP (2018) Soil basics, management, and rhizosphere engineering for sustainable agriculture. In: Channarayappa C, Biradar DP (eds) Abiotic stress: plants response to moisture and salt stresses. CRC Press, Boca RatonCrossRefGoogle Scholar
  22. Chattopadhyay MK, Gupta S, Sengupta DN, Ghosh B (1997) Expression of arginine decarboxylase in seedlings of indica rice (Oryza sativa L.) cultivars as affected by salinity stress. Plant Mol Biol 34:477–483PubMedCrossRefGoogle Scholar
  23. Chattopadhyay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199PubMedCrossRefGoogle Scholar
  24. Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384PubMedCrossRefGoogle Scholar
  25. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chen T, Li W, Hu X, Guo J, Liu A, Zhang B (2015) A cotton MYB transcription factor, GbMYB5, is positively involved in plant adaptive response to drought stress. Plant Cell Physiol 56:917–929.  https://doi.org/10.1093/pcp/pcv019CrossRefPubMedPubMedCentralGoogle Scholar
  27. Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945.  https://doi.org/10.3389/fpls.2018.01945CrossRefPubMedPubMedCentralGoogle Scholar
  28. Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499.  https://doi.org/10.1111/j.1744-7909.2009.00816.xCrossRefPubMedPubMedCentralGoogle Scholar
  29. Cheng X-Q, Zhu X-F, Tian W-G, Cheng W-H, Hakim SJ, Jin S-X, Zhu H-G (2017) Genome-wide identification and expression analysis of polyamine oxidase genes in upland cotton (Gossypium hirsutum L.). Plant Cell Tissue Organ Cult 129:237–249.  https://doi.org/10.1007/s11240-017-1172-0CrossRefGoogle Scholar
  30. Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33:1419–1438.  https://doi.org/10.1111/j.1365-3040.2010.02181.xCrossRefPubMedPubMedCentralGoogle Scholar
  31. de Oliveira LF, Elbl P, Navarro BV, Macedo AF, dos Santos ALW, Floh EIS (2017) Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol 37(1):116–130PubMedCrossRefPubMedCentralGoogle Scholar
  32. de Oliveira LF, Navarro BV, Cerruti GV, Elbl P, Minocha R, Minocha SC, dos Santos ALWS, Floh EIS (2018) Polyamine-and amino acid-related metabolism: the roles of arginine and ornithine are associated with the embryogenic potential. Plant Cell Physiol 59(5):1084–1098PubMedCrossRefPubMedCentralGoogle Scholar
  33. DeScenso RA, Minocha SC (1993) Modulation of cellular polyamines in tobacco by transfer and expression of a mouse ornithine decarboxylase cDNA. Plant Mol Biol 22:113–127CrossRefGoogle Scholar
  34. Diao Q-N, Song Y-J, Shi D-M, Qi H-Y (2016) Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling. J Zhejiang Univ Sci B 17:916–930.  https://doi.org/10.1631/jzus.B1600102CrossRefPubMedPubMedCentralGoogle Scholar
  35. Do PT, Drechsel O, Heyer AG, Hincha DK, Zuther E (2014) Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought. Front Plant Sci 5:182.  https://doi.org/10.3389/fpls.2014.00182CrossRefPubMedPubMedCentralGoogle Scholar
  36. Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635.  https://doi.org/10.1016/J.JPLPH.2007.11.006CrossRefPubMedPubMedCentralGoogle Scholar
  37. Duque AS, de Almeida AM, da Silva AB, da Silva JM, Farinha AP, Santos D, Fevereiro P, Araújo SS (2013) Abiotic stress responses in plants: unraveling the complexity of genes and networks to survive. In: Vahdati K, Leslie C (eds) Abiotic stress – plant responses and applications in agriculture. InTech, Rijeka, pp 49–101Google Scholar
  38. Duque AS, López-Gómez M, Kráčmarová J, Gomes CN, Araújo SS, Lluch C, Fevereiro P (2016) Genetic engineering of polyamine metabolism changes Medicago truncatula responses to water deficit. Plant Cell Tissue Organ Cult 127:681–690.  https://doi.org/10.1007/s11240-016-1107-1CrossRefGoogle Scholar
  39. Espasandin FD, Maiale SJ, Calzadilla P, Ruiz OA, Sansberro PA (2014) Transcriptional regulation of 9-cis-epoxycarotenoid dioxygenase (NCED) gene by putrescine accumulation positively modulates ABA synthesis and drought tolerance in Lotus tenuis plants. Plant Physiol Biochem 76:29–35.  https://doi.org/10.1016/J.PLAPHY.2013.12.018CrossRefPubMedPubMedCentralGoogle Scholar
  40. Espasandin FD, Calzadilla PI, Maiale SJ, Ruiz OA, Sansberro PA (2018) Overexpression of the arginine decarboxylase gene improves tolerance to salt stress in Lotus tenuis plants. J Plant Growth Regul 37:156–165.  https://doi.org/10.1007/s00344-017-9713-7CrossRefGoogle Scholar
  41. Falahi H, Sharifi M, Chashmi NA, Maivan HZ (2018) Water stress alleviation by polyamines and phenolic compounds in Scrophularia striata is mediated by NO and H2O2. Plant Physiol Biochem 130:139–147.  https://doi.org/10.1016/j.plaphy.2018.07.004CrossRefPubMedPubMedCentralGoogle Scholar
  42. Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant 31:937–945.  https://doi.org/10.1007/s11738-009-0307-2CrossRefGoogle Scholar
  43. Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic Biol Med 56:172–183PubMedCrossRefPubMedCentralGoogle Scholar
  44. Flemetakis E, Efrose R-C, Desbrosses G, Dimou M, Delis C, Aivalakis G, Udvardi M-K, Katinakis P (2004) Induction and spatial organization of polyamine biosynthesis during nodule development in Lotus japonicus. Mol Plant Microbe Interact 17:1283–1293PubMedCrossRefPubMedCentralGoogle Scholar
  45. Flores HE (1991) Changes in polyamine metabolism in response to abiotic stress. In: Slocum R, Flores HE (eds) The biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 214–225Google Scholar
  46. Flores HE, Galston A (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706PubMedPubMedCentralCrossRefGoogle Scholar
  47. Franceschetti M, Fornale S, Tassoni A, Zuccherelli K, Mayer MJ, Bagni N (2004) Effects of spermidine synthase over-expression on polyamine biosynthetic pathway in tobacco plants. J Plant Physiol 161:989–1001PubMedCrossRefPubMedCentralGoogle Scholar
  48. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5(1):26–33PubMedPubMedCentralCrossRefGoogle Scholar
  49. Gong B, Li X, Vanden Langenberg KM, Wen D, Sun S, Wei M, Li Y, Yang F, Shi Q, Wang X (2014) Overexpression of S-adenosyl- l -methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol J 12:694–708.  https://doi.org/10.1111/pbi.12173CrossRefPubMedPubMedCentralGoogle Scholar
  50. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45.  https://doi.org/10.1007/s00726-007-0501-8CrossRefPubMedPubMedCentralGoogle Scholar
  51. Grover A, Aggarwal PK, Kapoor A, Katiyar-Agarwal S, Agarwal M, Chandramouli A (2003) Addressing abiotic stresses in agriculture through transgenic technology. Curr Sci 84:355–367Google Scholar
  52. Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Front Plant Sci 7:1343.  https://doi.org/10.3389/fpls.2016.01343CrossRefPubMedPubMedCentralGoogle Scholar
  53. Hamill JD, Robins RJ, Parr AJ, Evan DM, Furze JM, Rhodes MJC (1990) Over-expression of a yeast ornithine decarboxylase gene in transgenic roots of Nicotiana rustica can lead to enhanced nicotine accumulation. Plant Mol Biol 15:27–38PubMedCrossRefPubMedCentralGoogle Scholar
  54. Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27:551–560PubMedCrossRefPubMedCentralGoogle Scholar
  55. Hanna WW (1995) Centipedegrass- diversity and vulnerability. Crop Sci 35:332–334.  https://doi.org/10.2135/cropsci1995.0011183X003500020007xCrossRefGoogle Scholar
  56. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256.  https://doi.org/10.1093/emboj/19.16.4248CrossRefPubMedPubMedCentralGoogle Scholar
  57. Harshavardhan VT, Govind G, Kalladan R, Sreenivasulu N, Hong C-Y (2018) Cross-protection by oxidative stress: improving tolerance to abiotic stresses including salinity. In: Kumar V, Wani S, Suprasanna P, Tran LS (eds) Salinity responses and tolerance in plants, vol 1. Springer International Publishing, Cham, pp 283–305CrossRefGoogle Scholar
  58. Hassan FAS, Ali EF, Alamer KH (2018) Exogenous application of polyamines alleviates water stress-induced oxidative stress of Rosa damascene Miller var. trigintipetala Dieck. S Afr J Bot 116:96–102CrossRefGoogle Scholar
  59. He L, Ban Y, Inoue H, Matsuda N, Liu J, Moriguchi T (2008) Enhancement of spermidine content and antioxidant capacity in transgenic pear shoots overexpressing apple spermidine synthase in response to salinity and hyperosmosis. Phytochemistry 69:2133–2141.  https://doi.org/10.1016/J.PHYTOCHEM.2008.05.015CrossRefPubMedPubMedCentralGoogle Scholar
  60. He M, He C-Q, Ding N-Z (2018) Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci 9:1771.  https://doi.org/10.3389/fpls.2018.01771CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ikbal FE, Hernández JA, Barba-Espín G, Koussa T, Aziz A, Faize M, Diaz-Vivancos P (2014) Enhanced salt-induced antioxidative responses involve a contribution of polyamine biosynthesis in grapevine plants. J Plant Physiol 171:779–788.  https://doi.org/10.1016/j.jplph.2014.02.006CrossRefPubMedPubMedCentralGoogle Scholar
  62. Islam MA, Hirata M (2005) Centipedegrass (Eremochloa ophiuroides (Munro) Hack.): growth behavior and multipurpose usages. Grassl Sci 51:183–190.  https://doi.org/10.1111/j.1744-697X.2005.00014.xCrossRefGoogle Scholar
  63. Kakkar RK, Sawhney VK (2002) Polyamine research in plants – a changing perspective. Physiol Plant 116:281–292.  https://doi.org/10.1034/j.1399-3054.2002.1160302.xCrossRefGoogle Scholar
  64. Kasinathan V, Wingler A (2002) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107CrossRefGoogle Scholar
  65. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722PubMedCrossRefPubMedCentralGoogle Scholar
  66. Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83.  https://doi.org/10.5511/plantbiotechnology.23.75CrossRefGoogle Scholar
  67. Khare T, Srivastav A, Shaikh S, Kumar V (2018) Polyamines and their metabolic engineering for plant salinity stress tolerance. In: Kumar V, Wani S, Suprasanna P, Tran LS (eds) Salinity responses and tolerance in plants, vol 1. Springer International Publishing, Cham, pp 339–358CrossRefGoogle Scholar
  68. Kolotilin I, Koltai H, Bar-Or C, Chen L, Nahon S, Shlomo H, Levin I, Reuveni M (2011) Expressing yeast SAMdc gene confers broad changes in gene expression and alters fatty acid composition in tomato fruit. Physiol Plant 142:211–223.  https://doi.org/10.1111/j.1399-3054.2011.01458.xCrossRefPubMedPubMedCentralGoogle Scholar
  69. Kumar A, Taylor MA, Arif SAM, Davies HV (1996) Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J 9:147–158.  https://doi.org/10.1046/j.1365-313X.1996.09020147.xCrossRefGoogle Scholar
  70. Kumar A, Altabella T, Taylor MA, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2:124–130CrossRefGoogle Scholar
  71. Kumar RR, Sharma SK, Rai GK, Singh K, Choudhury M, Gaurav D, Singh GP, Goswami S, Pathak H, Rai RD (2014) Exogenous application of putrescine at pre-anthesis enhances the thermotolerance of wheat (Triticum aestivum L.). Indian J Biochem Biophys 51(5):396–406PubMedPubMedCentralGoogle Scholar
  72. Kumar V, Wani SH, Suprasanna P, Tran L-SP (eds) (2018) Salinity responses and tolerance in plants. Volume 1, Targeting sensory, transport and signaling mechanisms. Springer International Publishing, Cham.  https://doi.org/10.1007/978-3-319-75671-4CrossRefGoogle Scholar
  73. Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamine metabolism, in vitro morphogenesis and response to salt stress. J Plant Physiol 159:983–990CrossRefGoogle Scholar
  74. Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:1–14.  https://doi.org/10.3389/fchem.2018.00026CrossRefGoogle Scholar
  75. Lesins K, Lesins I (1979) Genus Medicago (Leguminosae): a taxogenetic study. Junk Publishers, The Hague.  https://doi.org/10.1007/978-94-009-9634-2CrossRefGoogle Scholar
  76. Li K, Xing C, Yao Z, Huang X (2017) PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol J 15(9):1186–1203.  https://doi.org/10.1111/pbi.12708CrossRefPubMedPubMedCentralGoogle Scholar
  77. Liu J-H, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126CrossRefGoogle Scholar
  78. Liu YH, Offler CE, Ruan YL (2013) Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Front Plant Sci 4:282.  https://doi.org/10.3389/fpls.2013.00282CrossRefPubMedPubMedCentralGoogle Scholar
  79. Liu J-H, Wang W, Wu H, Gong X, Moriguchi T (2015a) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827.  https://doi.org/10.3389/fpls.2015.00827CrossRefPubMedPubMedCentralGoogle Scholar
  80. Liu M, Chu M, Ding Y, Wang S, Liu Z, Tang S, Ding C, Li G (2015b) Exogenous spermidine alleviates oxidative damage and reduce yield loss in rice submerged at tillering stage. Front Plant Sci 6:919.  https://doi.org/10.3389/fpls.2015.00919CrossRefPubMedPubMedCentralGoogle Scholar
  81. Lu S, Zhuo C, Wang X, Guo Z (2014) Nitrate reductase (NR)-dependent NO production mediates ABA- and H2O2-induced antioxidant enzymes. Plant Physiol Biochem 74:9–15.  https://doi.org/10.1016/J.PLAPHY.2013.10.030CrossRefPubMedPubMedCentralGoogle Scholar
  82. Luo J, Liu M, Zhang C, Peipei Z, Jingjing C, Zhenfei G, Shaoyun L (2017) Transgenic centipedegrass (Eremochloa ophiuroides [Munro] Hack.) overexpressing S-adenosylmethionine decarboxylase (SAMDC) gene for improved cold tolerance through involvement of H2O2 and NO signaling. Front Plant Sci 8:1655.  https://doi.org/10.3389/fpls.2017.01655CrossRefPubMedPubMedCentralGoogle Scholar
  83. Lutts S, Hausman JF, Quinet M, Lefèvre I (2013) Polyamines and their roles in the alleviation of ion toxicities in plants. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 315–353CrossRefGoogle Scholar
  84. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466.  https://doi.org/10.1146/annurev.pp.24.060173.002305CrossRefGoogle Scholar
  85. Majumdar R, Barchi B, Turlapati AS, Gagne M, Minocha R, Long S, Minocha SC (2016) Glutamate, ornithine, arginine, proline, and polyamine metabolic interactions: the pathway is regulated at the post-transcriptional level. Front Plant Sci 7:78PubMedPubMedCentralCrossRefGoogle Scholar
  86. Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34:135–148CrossRefGoogle Scholar
  87. Masgrau C, Altabella T, Farras R, Flores D, Thompson AJ, Besford RT, Tiburcio AF (1997) Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants. Plant J 11:465–473.  https://doi.org/10.1046/j.1365-313X.1997.11030465.xCrossRefPubMedGoogle Scholar
  88. Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy based metabolite profiles of transgenic tomato fruit engineered to accumulate polyamines spermidine and spermine reveal enhanced anabolic nitrogen-carbon interactions. Plant Physiol 142(4):1759–1770PubMedPubMedCentralCrossRefGoogle Scholar
  89. Mattoo AK, Fatima T, Upadhyay RK, Handa AK (2014) Polyamines in plants: biosynthesis from arginine, and metabolic, physiological, and stress-response roles. In: D’Mello JPF (ed) Polyamine biosynthesis in plants. CAB International, Wallingford, pp 177–194Google Scholar
  90. Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality and vine life. Nat Biotechnol 20(6):613–618PubMedCrossRefPubMedCentralGoogle Scholar
  91. Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci 6:419PubMedPubMedCentralCrossRefGoogle Scholar
  92. Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175PubMedPubMedCentralCrossRefGoogle Scholar
  93. Mohammadi H, Ghorbanpour M, Brestic M (2018) Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind Crop Prod 122:119–132CrossRefGoogle Scholar
  94. Mohapatra S, Minocha R, Long S, Subhash C, Minocha SC (2009) Putrescine overproduction negatively impacts the oxidative state of poplar cells in culture. Plant Physiol Biochem 47:262–271PubMedCrossRefGoogle Scholar
  95. Moschou PN, Paschalidis AKA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3(12):1061–1066PubMedPubMedCentralCrossRefGoogle Scholar
  96. Nayyar H, Kaur S, Singh K, Kumar S, Singh KJ, Dhir KK (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L.) Merrill.) to water deficit stress. Bot Bull Acad Sci 46:333–338Google Scholar
  97. Ndayiragije A, Lutts S (2006) Exogenous putrescine reduces sodium and chloride accumulation in NaCl-treated calli of the salt-sensitive rice cultivar I Kong Pão. Plant Growth Regul 48:51–63CrossRefGoogle Scholar
  98. Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11.  https://doi.org/10.1093/aob/mcw191CrossRefPubMedGoogle Scholar
  99. Nunes C, Araújo SS, da Silva JM, Fevereiro MPS, da Silva AB (2008) Physiological responses of the legume model Medicago truncatula cv. Jemalong to water deficit. Environ Exp Bot 63:289–296.  https://doi.org/10.1016/j.envexpbot.2007.11.004CrossRefGoogle Scholar
  100. Page AF, Minocha R, Minocha SC (2012) Living with high putrescine: expression of ornithine and arginine biosynthetic pathway genes in high and low putrescine producing poplar cells. Amino Acids 42(1):295–308PubMedCrossRefGoogle Scholar
  101. Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23.  https://doi.org/10.1016/J.PLANTSCI.2015.05.003CrossRefPubMedGoogle Scholar
  102. Pandey R, Gupta A, Chowdhary A, Pal RK, Rajam MV (2015) Over-expression of mouse ornithine decarboxylase gene under the control of fruit-specific promoter enhances fruit quality in tomato. Plant Mol Biol 87:249–260.  https://doi.org/10.1007/s11103-014-0273-yCrossRefPubMedPubMedCentralGoogle Scholar
  103. Pang C, Wang C, Chen H, Guo Z, Li C (2009) Transcript profiling of cold responsive genes in Medicago falcata. In: Yamada T, Spangenberg G (eds) Molecular breeding of forage and turf. Springer New York, New York, pp 141–150CrossRefGoogle Scholar
  104. Patel J, Ariyaratne M, Ahmed S, Ge L, Phuntumart V, Kalinoski A, Morris PF (2017) Dual functioning of plant arginases provides a third route for putrescine synthesis. Plant Sci 262:62–73PubMedCrossRefPubMedCentralGoogle Scholar
  105. Pathak MR, Teixeira da Silva JA, Wani SH (2014) Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food 5:87–96.  https://doi.org/10.4161/gmcr.28774CrossRefPubMedPubMedCentralGoogle Scholar
  106. Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol 70:253–264.  https://doi.org/10.1007/s11103-009-9470-5CrossRefPubMedPubMedCentralGoogle Scholar
  107. Podlešáková K, Ugena L, Spíchal L, Doležal K, De Diego N (2018) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 25:53–65Google Scholar
  108. Prabhavathi VR, Rajam MV (2007) Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol 24:273–282.  https://doi.org/10.5511/plantbiotechnology.24.273CrossRefGoogle Scholar
  109. Prabhavathi V, Yadav JS, Kumar PA, Rajam MV (2002) Abiotic stress tolerance in transgenic eggplant (Solanum melongena L.) by introduction of bacterial mannitol phosphodehydrogenase gene. Mol Breed 9:137–147.  https://doi.org/10.1023/A:1026765026493CrossRefGoogle Scholar
  110. Purushothaman R, Krishnamurthy L, Upadhyaya HD, Vadez V, Varshney RK (2017) Genotypic variation in soil water use and root distribution and their implications for drought tolerance in chickpea. Funct Plant Biol 44:235–252.  https://doi.org/10.1071/FP16154CrossRefGoogle Scholar
  111. Radhakrishnan R, Lee I (2013) Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J Plant Growth Regul 32:22–30CrossRefGoogle Scholar
  112. Rady MM, El-Yazal MAS, Taie HAA, Ahmed SMA (2016) Response of wheat growth and productivity to exogenous polyamines under lead stress. J Crop Sci Biotechnol 19:363–371.  https://doi.org/10.1007/s12892-016-0041-4CrossRefGoogle Scholar
  113. Romero FM, Maiale SJ, Rossi FR, Marina M, Ruíz OA, Gárriz A (2018) Polyamine metabolism responses to biotic and abiotic stress. In: Alcázar R, Tiburcio A (eds) Polyamines. Methods in molecular biology, vol 1694. Humana Press, New York, pp 37–49Google Scholar
  114. Rosenzweig C, Iglesias A, Yang XB, Epstein PR, Chivian E (2001) Climate change and extreme weather events; implications for food production, plant diseases, and pests. Glob Change Hum Health 2:90–104.  https://doi.org/10.1023/A:1015086831467CrossRefGoogle Scholar
  115. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875.  https://doi.org/10.1016/S0168-9452(01)00337-5CrossRefPubMedPubMedCentralGoogle Scholar
  116. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992.  https://doi.org/10.1016/S0168-9452(02)00272-8CrossRefGoogle Scholar
  117. Ruelland E, Vaultier M-N, Zachowski A, Hurry V (2009) Chapter 2: Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150.  https://doi.org/10.1016/S0065-2296(08)00602-2CrossRefGoogle Scholar
  118. Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Front Environ Sci 3:21.  https://doi.org/10.3389/fenvs.2015.00021CrossRefGoogle Scholar
  119. Santa-Catarina C, Silveira V, Scherer GF, Floh EIS (2007) Polyamine and nitric oxide levels relate with morphogenetic evolution in somatic embryogenesis of Ocotea catharinensis. Plant Cell Tissue Organ Cult 90(1):93–101CrossRefGoogle Scholar
  120. Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant Cell Environ 23:719–726.  https://doi.org/10.1046/j.1365-3040.2000.00589.xCrossRefGoogle Scholar
  121. Sato S, Peet MM, Gardner RG (2001) Formation of parthenocarpic fruit, undeveloped flowers and aborted flowers in tomato under moderately elevated temperatures. Sci Hortic (Amsterdam) 90:243–254.  https://doi.org/10.1016/S0304-4238(00)00262-4CrossRefGoogle Scholar
  122. Seifi HS, Shelp BJ (2019) Spermine differentially refines plant defense responses against biotic and abiotic stresses. Front Plant Sci 10:117.  https://doi.org/10.3389/fpls.2019.00117CrossRefPubMedPubMedCentralGoogle Scholar
  123. Serafini-Fracassini D, Del Duca S (2008) Transglutaminases: widespread crosslinking enzymes in plants. Ann Bot 102:145–152PubMedPubMedCentralCrossRefGoogle Scholar
  124. Silveira V, Santa-Catarina C, Tun NN, Scherer GFE, Handro W, Guerra MP, Floh EIS (2006) Polyamine effects on the endogenous polyamine contents, nitric oxide release, growth and differentiation of embryogenic suspension cultures of Araucaria angustifolia (Bert.) O. Ktze. Plant Sci 171(1):91–98CrossRefGoogle Scholar
  125. Sun P, Zhu X, Huang X, Liu J-H (2014) Overexpression of a stress-responsive MYB transcription factor of Poncirus trifoliata confers enhanced dehydration tolerance and increases polyamine biosynthesis. Plant Physiol Biochem 78:71–79.  https://doi.org/10.1016/j.plaphy.2014.02.022CrossRefPubMedPubMedCentralGoogle Scholar
  126. Tajti J, Janda T, Majláth I, Szalai G, Pál M (2018) Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol Environ Saf 148:546–554PubMedCrossRefPubMedCentralGoogle Scholar
  127. Talaat NB, Shawky BT, Ibrahim AS (2015) Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environ Exp Bot 113:47–58CrossRefGoogle Scholar
  128. Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37(4):864–885PubMedCrossRefPubMedCentralGoogle Scholar
  129. Tardieu F, Simonneau T, Muller B (2018) The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu Rev Plant Biol 69:733–759.  https://doi.org/10.1146/annurev-arplant-042817-040218CrossRefPubMedPubMedCentralGoogle Scholar
  130. Tiburcio AF, Alcázar R (2018) Potential applications of polyamines in agriculture and plant biotechnology. In: Alcázar R, Tiburcio A (eds) Polyamines: methods in molecular biology, volume 1694. Humana Press, New YorkGoogle Scholar
  131. Tiburcio AF, Altabella T, Borrell A, Masgrau C (1997) Polyamine metabolism and its regulation. Physiol Plant 100(3):664–674CrossRefGoogle Scholar
  132. Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47(3):346–354PubMedCrossRefPubMedCentralGoogle Scholar
  133. Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi K, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926CrossRefGoogle Scholar
  134. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375PubMedCrossRefPubMedCentralGoogle Scholar
  135. Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734CrossRefGoogle Scholar
  136. Wang W, Liu J-H (2016) CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress. Sci Rep 6:31384.  https://doi.org/10.1038/srep31384CrossRefPubMedPubMedCentralGoogle Scholar
  137. Wen X-P, Pang X-M, Matsuda N, Kita M, Inoue H, Hao Y-J, Honda C, Moriguchi T (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263.  https://doi.org/10.1007/s11248-007-9098-7CrossRefPubMedPubMedCentralGoogle Scholar
  138. Wen X-P, Ban Y, Inoue H, Matsuda N, Moriguchi T (2009) Aluminum tolerance in a spermidine synthase-overexpressing transgenic European pear is correlated with the enhanced level of spermidine via alleviating oxidative status. Environ Exp Bot 66:471–478.  https://doi.org/10.1016/J.ENVEXPBOT.2009.03.014CrossRefGoogle Scholar
  139. Wen X-P, Ban Y, Inoue H, Matsuda N, Moriguchi T (2010) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103.  https://doi.org/10.1007/s11248-009-9296-6CrossRefPubMedPubMedCentralGoogle Scholar
  140. Wen X-P, Ban Y, Inoue H, Matsuda N, Kita M, Moriguchi T (2011) Antisense inhibition of a spermidine synthase gene highlights the role of polyamines for stress alleviation in pear shoots subjected to salinity and cadmium. Environ Exp Bot 72:157–166.  https://doi.org/10.1016/J.ENVEXPBOT.2011.03.001CrossRefGoogle Scholar
  141. Wimalasekera R, Tebartz F, Scherer GF (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181(5):593–603PubMedCrossRefPubMedCentralGoogle Scholar
  142. Wu Y, Zhou H, Que Y-X, Chen R-K, Zhang M-Q (2008) Cloning and identification of promoter Prd29A and its application in sugarcane drought resistance. Sugar Tech 10:36–41.  https://doi.org/10.1007/s12355-008-0006-0CrossRefGoogle Scholar
  143. Wuddineh W, Minocha R, Minocha SC (2018) Polyamines in the context of metabolic networks. In: Alcázar R, Tiburcio AF (eds) Polyamines: methods and protocols. Humana Press, New York, pp 1–23Google Scholar
  144. Xu W, Cui K, Xu A, Nie L, Huang J, Peng S (2015) Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiol Plant 37:9.  https://doi.org/10.1007/s11738-014-1760-0CrossRefGoogle Scholar
  145. Xu J, Wolters-Arts M, Mariani C, Huber H, Rieu I (2017) Heat stress affects vegetative and reproductive performance and trait correlations in tomato (Solanum lycopersicum). Euphytica 213:156.  https://doi.org/10.1007/s10681-017-1949-6CrossRefGoogle Scholar
  146. Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Dev 30:515–527.  https://doi.org/10.1051/agro/2009050CrossRefGoogle Scholar
  147. Yadav JS, Rajam MV (1997) Spatial distribution of free and conjugated polyamines in leaves of Solanum melongena L. associated with differential morphogenetic capacity: efficient somatic embryogenesis with putrescine. J Exp Bot 48(8):1537–1545CrossRefGoogle Scholar
  148. Yang W, Li Y, Yin Y, Qin Z, Zheng M, Chen J, Luo Y, Pang D, Jiang W, Li Y, Wang Z (2017) Involvement of ethylene and polyamines biosynthesis and abdominal phloem tissues characters of wheat caryopsis during grain filling under stress conditions. Sci Rep 7:46020.  https://doi.org/10.1038/srep46020CrossRefPubMedPubMedCentralGoogle Scholar
  149. Ye B, Muller HH, Zhang J, Gressel J (1998) Constitutively elevated levels of putrescine and putrescine generating enzymes correlated with oxidant stress resistance in Conyza bonariensis and wheat. Plant Physiol 115:1443–1451CrossRefGoogle Scholar
  150. Yin L, Wang S, Tanaka K, Fujihara S, Itai A, Den X, Zhang S (2016) Silicon-mediated changes in polyamines participate in silicon-induced salt tolerance in Sorghum bicolor L. Plant Cell Environ 39:245–258PubMedCrossRefPubMedCentralGoogle Scholar
  151. Zapata PJ, Serrano M, García-Legaz MF, Pretel MT, Botella MA (2017) Short term effect of salt shock on ethylene and polyamines depends on plant salt sensitivity. Front Plant Sci 8:855.  https://doi.org/10.3389/fpls.2017.00855CrossRefPubMedPubMedCentralGoogle Scholar
  152. Zeid IM, Shedeed ZA (2006) Response of alfalfa to putrescine treatment under drought stress. Biol Plant 50(4):635–640CrossRefGoogle Scholar
  153. Zhang Y, Zhang H, Zou ZR, Liu Y, Hu XH (2015) Deciphering the protective role of spermidine against saline-alkaline stress at physiological and proteomic levels in tomato. Phytochemistry 110:13–21PubMedCrossRefPubMedCentralGoogle Scholar
  154. Zhuo C, Liang L, Zhao Y, Guo Z, Lu S (2018) A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation. Plant Cell Environ 41:2021–2032.  https://doi.org/10.1111/pce.13114CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Susana de Sousa Araújo
    • 1
  • André Luis Wendt dos Santos
    • 2
  • Ana Sofia Duque
    • 1
    Email author
  1. 1.Laboratory of Plant Cell Biotechnology (BCV), Instituto de Tecnologia Química e Biológica António Xavier (Green-it Unit)Universidade Nova de LisboaOeirasPortugal
  2. 2.Laboratory of Plant Cellular Biology (BIOCEL), Instituto de Biociências (IB)Universidade de São Paulo (USP)São PauloBrazil

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