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Polyamines Contribution to the Improvement of Crop Plants Tolerance to Abiotic Stress

  • Ana Bernardina Menéndez
  • Andrés Alberto Rodriguez
  • Santiago Javier Maiale
  • Kessler Margarita Rodriguez
  • Bremont Juan Francisco Jimenez
  • Oscar Adolfo RuizEmail author
Chapter

Abstract

Plant development and productivity are negatively regulated by environmental stresses. The loss of productivity is triggered by a series of morphological, physiological, biochemical and molecular stress-induced changes. The development of diverse strategies to obtain stress-tolerant plants is currently one of the most active fields in plant research, which is expected to help prevent the dramatic reduction in crop yields due to global climate changing effects. Therefore, the identification of stress-regulatory genes and signaling molecules involved in the process of stress tolerance should allow the development of novel strategies to obtain tolerant plants. Polyamines (PAs) are polycationic compounds with a recognized role in plant growth and development, as well as in abiotic and biotic stress responses. In this chapter, we review and discuss the information concerning the modifications in polyamines levels in response to drought, salinity and cold stresses, focusing on crop species. The comparison of common and specific responses in different crop plants suggests the view that polyamines actively participate in stress signaling through an intricate metabolic network. However, the precise mechanism(s) of action by which PAs could protect crop plants from challenging environmental conditions remains unclear.

Keywords

Abiotic stress tolerance Cold Crop improvement Drought Polyamines biosynthesis Polyamine catabolism Salt 

Notes

Acknowledgements

This work was supported by grants from PICT of Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT, Argentina), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina), San Martin University (UNSAM) to OAR. OAR also acknowledges grants-in-aid from COST-Action FA0605. MEG and FDE are fellows of CONICET (Argentina). ABM, SJM, AAR and OAR are members of the research committee from CONICET (Argentina).

References

  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Planta 231:1237–1249Google Scholar
  2. Allan AC, Fricker MD, Ward JL, Beale MH, Trewavas AJ (1994) Plant Cell 6:1319–1328Google Scholar
  3. Anderson BE, Ward JM, Schroeder JI (1994) Plant Physiol 104:1177–1183Google Scholar
  4. Antognoni F, Fornalè S, Grimmer C, Komor E, Bagni N (1998) Planta 204:520–527Google Scholar
  5. Antolín MC, Santesteban H, Santa María E, Aguirreolea J, Sánchez-Díaz M (2008) Aust J Grape Wine Res 14:123–133Google Scholar
  6. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubis J (2009) J Plant Growth Regul 28:177–186Google Scholar
  7. Bae H, Kim S-H, Kim MS, Sicher RC, Lary D, Strem MD, Natarajan S, Bailey BA (2008) Plant Physiol Biochem 46:174–188Google Scholar
  8. Bagni N, Pistocchi R (1991) In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants, CRC press, Boca Raton, FL, pp 105–120Google Scholar
  9. Bagni N, Tassoni A (2001) Amino Acids, 20:301–317Google Scholar
  10. Baigorri H, Antolín MC, De Luis I, Geny L, Broquedis M, Aguirrezábal F, Sánchez Díaz M (2001) Am J Enol Vitic 52:357–363Google Scholar
  11. Basu S, Roychoudhury A, Saha PP, Sengupta DN (2010) Acta Physiol Plant 32:551–563Google Scholar
  12. Besford RT, Richardson CM, Campos JL, Tiburcio AF (1993) Planta 189:201–206Google Scholar
  13. Borrell A, Culianez-Macia F, Altabella T, Besford R, Flores D, Tiburcio A (1995) Plant Physiol 109:771–776Google Scholar
  14. Bortolotti C, Cordeiro A, Alcázar R, Borrell A, Culiañez-Macià FA, Tiburcio AF, Altabella T (2004) Physiol Plant 120:84–92Google Scholar
  15. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Plant Sci 140:103–125Google Scholar
  16. Caffaro SV, Vicente C (1994) Plant Physiol Biochem 32:391–397Google Scholar
  17. Campestre MP, Bordenave CD, Origone AC, Menéndez AB, Ruiz OA, Rodríguez AA, Maiale SJ (2011) J Plant Physiol 168:1234–1240Google Scholar
  18. Capell T, Bassie L, Christou P (2004) PNAS 101:9909–9914Google Scholar
  19. Cervelli M, Di Caro O, Di Penta A, Angelini R, Federico R, Vitale A, Mariottini P (2004) Plant J 40:410–418Google Scholar
  20. Chattopadhyay MK, Gupta S, Sengupta DN, Ghosh B (1997) Plant Mol Biol 34:477–483Google Scholar
  21. Chattopadhyay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Physiol Plant 116:192–199Google Scholar
  22. Chen W, Provart NJ, Glazebrook J (2002) Plant Cell 14:559–574Google Scholar
  23. Chen WP, Li PH (2002) In: Li C, Palva ET (eds) Plant cold hardiness, Kluwer Academic Publishers, Dordrecht, NL, pp 223–233Google Scholar
  24. Childs AC, Mehta DJ, Gerner EW (2003) Cell Mol Life Sci 60:1394–1406Google Scholar
  25. Cona A, Cenci F, Cervelli M, Fedrico R, Mariottini P, Moreno S, Angelini R (2003) Plant Physiol 110:137–145Google Scholar
  26. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Trends Plant Sci 11:80–88Google Scholar
  27. Cuevas JC, Lopez-Cobollo R, Alcàzar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Plant Physiol 148:1094–1105Google Scholar
  28. Del Duca H, Beninati S, Serafini-Fracassini D (1995) Biochem J 305:233–237Google Scholar
  29. Delauney AJ, Verma DPS (1993) Plant J 4:215–223Google Scholar
  30. Demidchik V, Maathuis FJM (2007) New Phytol 175:387–404Google Scholar
  31. Di Tomaso lM, Hart JJ, Kochian LV (1992) Plant Physiol 98:611–620Google Scholar
  32. Dondini L, Del Duca S, Dall’Agata L, Bassi R, Gastaldelli M, Della Mea M, Di Sandro A, Claparols I, Serafini-Fracassini D (2003) Planta 217:84–95Google Scholar
  33. Edreva AM, Velikova VB, Tsonev TD (2007) Russ J Plant Physiol 54:287–301Google Scholar
  34. El-bassiouny HMS, Bekheta MA (2005) Int J Agric Biol 7:363–368Google Scholar
  35. El-Shintinawy F (2000) Photosynthetica 38:615–620Google Scholar
  36. Erdei L, Szegletes Z, Barabás K, Pestenácz A (1996) J Plant Physiol 147:599–603Google Scholar
  37. Evers D, Lefèvre I, Legay S, Lamoureux D, Hausman J-F, Gutierrez Rosales RO, Tincopa Marca LP, Hoffmann L, Bonierbale M, Schafleitner R (2010) J Exp Bot 61:2327–2343Google Scholar
  38. Farooq M, Wahid A, Lee DJ (2009) Acta Physiol Plant 31:937–945Google Scholar
  39. Federico R, Angelini R (1991) In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants, CRS Press, Boca Raton, FL, pp 41–56Google Scholar
  40. Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2011) J Exp Bot 62:1155–1168Google Scholar
  41. Flores HE, Galston AW (1984) Plant Physiol 75:102–109Google Scholar
  42. Flores HE, Martin-Tanguy J (1991) In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants, CRS Press, Boca Raton, FL, pp 57–76Google Scholar
  43. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Nature, 422:442–446Google Scholar
  44. Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Plant Physiol Biochem 48:513–520Google Scholar
  45. Fujihara S, Abe H, Yoneyama T (1995) J Biol Chem 270:9932–9938Google Scholar
  46. Galston AW, Sawhney RK (1990) Plant Physiol 94:406–410Google Scholar
  47. Gao C, Hu J, Zhang S, Zheng Y, Knapp A (2009) Plant Growth Reg 57:31–38Google Scholar
  48. Garcia-Mata C, Lamattina L (2001) Plant Physiol 126:1196–1204Google Scholar
  49. García-Mata C, Lamattina L (2002) Plant Physiology 128:790–792Google Scholar
  50. Geny L, Colin L, Brazillon I, Broquedis M (1999) Vitis 38:157–160Google Scholar
  51. Ghosh N, Adak MK, Ghosh PD, Gupta S, Gupta DNS, Mandal C (2011) Plant Biotech Rep 5:89–103Google Scholar
  52. Gill SS, Tuteja N (2010) Plant Signal Behav 5:26–33Google Scholar
  53. Groppa MD, Benavides MP (2008) Amino Acids 34:35–45Google Scholar
  54. Guye MG, Vigh L, Wilson JL (1986) J Exp Bot 37:1036–1043Google Scholar
  55. Handa AK, Mattoo AK (2010) Plant Physiol Biochem 487:540–546Google Scholar
  56. Hanzawa Y, Takahashi T, Michael J (2000) EMBO J 19:4248–4256Google Scholar
  57. Hart JJ, DiTomaso JM, Linscott DL, Kochian LV (1992) Plant Physiol 99:1400–1405Google Scholar
  58. Hazarika P, Rajam MV (2011) Physiol Mol Biol Plants 17:115–128Google Scholar
  59. He L, Nada K, Tachibana S (2002) J Jpn Soc Hortic Sci 71:490–498Google Scholar
  60. He L, Ban Y, Inoue H, Matsuda N, Liu JM (2008) Phytochem 69:2133–2141Google Scholar
  61. Hummel I, Couée I, Amrani A, Martin-Tanguy J, Hennion F (2002) J Exp Bot 53:1463–1473Google Scholar
  62. Igarashi K, Kashiwagi K (2000) Biochem Biophys Res Commun 271:559–564Google Scholar
  63. Illingworth C, Mayer MJ, Elliott K, Hanfrey C, Walton NJ, Michael AJ (2000) FEBS Lett 549:26–30Google Scholar
  64. Imai R, Ali A, Pramanik MdHR, Nakaminami K, Sentoku N, Kato H (2004) J Plant Physiol 161:883–886Google Scholar
  65. Islam MA, Blake T, Kocacinar F, Lada R (2003) Trees 17:278–284Google Scholar
  66. Janská A, Maršík P, Zelenková S, Ovesná J (2010) Plant Biol 12:395–405Google Scholar
  67. Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Plant Physiol Biochem 45:812–821Google Scholar
  68. Kakkar RK, Nagar PK, Ahuja PS, Rai VK (2000) Biolo Plant 43:1–11Google Scholar
  69. Kakkar RK, Sawney YK (2002) Physiol Plant 116:281–292Google Scholar
  70. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) Plant Cell Physiol 49:1272–1282Google Scholar
  71. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Plant and Cell Physiology 45:712–722Google Scholar
  72. Kasukabe, Y, He L,Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Plant Biotechnology 23:75–83Google Scholar
  73. Kim TE, Kim SK, Han TJ, Lee JS, Chang SC (2002) Physiol Plant 115:370–376Google Scholar
  74. Knott JM, Römer P, Sumper M (2007) FEBS Lett 581:3081–3086Google Scholar
  75. Kotzabasis K, Fotinou C, Roubelakis-Angelakis KA, Ghanotakis D (1993) Photosynth Res 38:83–88Google Scholar
  76. Krishnamurthy R, Bhagwat KA (1989) Plant Physiol 91:500–504Google Scholar
  77. Kubis J (2008) J Plant Physiol 165:397–406Google Scholar
  78. Kuehn GO, Bagga S, Rodriguez-Garay B, Philipps AC (1990) In: Flores HE, Arteca RN, Shannon JC (eds) Polyamines and ethylene: Biochemistry, physiology and interactions, American Society of Plant Physiology, pp 190–202Google Scholar
  79. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Planta 228:367–381Google Scholar
  80. Kuznetsov V, Radukina NL, Shevyakoval NI (2007) Metabolism of polyamines and prospects for producing stress-tolerant plants: An overview. In: Thangadurai D, Tang W, Song S-Q (eds) Plant stress and biotechnology, Oxford Book Company, Jaipur, India, p 257Google Scholar
  81. Laurenzi M, Rea G, Federico R, Tavladoraki P, Angelini R (1999) Planta 208:146–154Google Scholar
  82. Laurenzi M, Tipping AJ, Marcus SE, Knox JP, Federico R, Angelini R, McPherson MJ (2001) Planta 214:37–45Google Scholar
  83. Lee TM, Lur HS, Chu C (1995) Crop Sci 35:502–508Google Scholar
  84. Lee TM, Lur HS, Chu C (1997) Plant Sci 126:1–10Google Scholar
  85. Legocka J, Kluk A (2005) J Plant Physiol 162:662–668Google Scholar
  86. Lei Y (2008) Russ J Plant Physiol 55:857–864Google Scholar
  87. Lester GE (2000) Plant Sci 160:105–112Google Scholar
  88. Li CZ, Jiao J, Wang GX (2004) Plant Sci 166:303–315Google Scholar
  89. Li ZY, Chen SY (2000) Theor Appl Genet 100:782–788Google Scholar
  90. Liu H, Liu Y, Yu B, Liu Z, Zhang W (2004) J Plant Growth Reg 23:156–165Google Scholar
  91. Liu H, Nakajima I, Moriguchi T (2011) Biol Plant 55:340–344Google Scholar
  92. Liu HH, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Plant Sci 166:1261–1267Google Scholar
  93. Liu HP, Yu BJ, Zhang WH, Liu YL (2005) Plant Sci 168:1599–1607Google Scholar
  94. Liu J, Yu B-J, Liu Y-L (2006) Plant Growth Reg 49:119–126Google Scholar
  95. Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Plant Biotech 24:117–126Google Scholar
  96. Liu JH, Nakajima I, Moriguchi T (2011) Biol Plant 55:340–344Google Scholar
  97. Livingston DP, Premakumar R, Tallury SP (2006) Cryobiology 52:200–208Google Scholar
  98. Maiale S, Sanchez DH, Guirado A, Vidal A, Ruiz O (2004) J Plant Physiol 161:35–42Google Scholar
  99. Mansour MMF, Al-Mutawa MM (1999) Cytobios 100:7–17Google Scholar
  100. Mariani P, D’Orazi D, Bagni N (1989) J Plant Physiol 135:508–510Google Scholar
  101. Martin-Tanguy J (1997) Physiol Plant 100:675–688Google Scholar
  102. Medda R, Padiglia A, Pedersen JZ, Rotilio G, Finazzi Agrò A, Floris G (1995) Biochem 34:16375–16381Google Scholar
  103. Moller SG, McPherson MJ (1998) Plant J 13:781–791Google Scholar
  104. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Plant Cell 20:1708–1724Google Scholar
  105. Nadeau P, Delaney S, Chouinard L (1987) Plant Physiol 84:73–77Google Scholar
  106. Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai MA, Kusano T, Takahashi Y (2010) Plant Physiol Biochem 48:527–533Google Scholar
  107. Nayyar H, Chander S (2004) J Agr Crop Sci 190:355–365Google Scholar
  108. Nayyar H (2005) J Agr Crop Sci 191:340–345Google Scholar
  109. Németh M, Janda T, Horváth E, Páldi E, Szalai G (2002) Plant Sci 162:569–574Google Scholar
  110. Oufir M, Legay S, Nicot N, Van Moer K, Hoffmann L, Renaut J, Hausman JF, Evers D (2008) Plant Sci 175:839–852Google Scholar
  111. Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Plant Mol Biol 48:551–573Google Scholar
  112. Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Plant Cell Physiol 51:422–434Google Scholar
  113. Pang JY, Long YH, Chen WH, Jiang ZH (2007) Bioorg Med Chem Lett 17:1018–1021Google Scholar
  114. Pang X-M, Zhang Z-Y, Wen X-P, Ban Y, Moriguchi T. Plant Stress 1:173–188Google Scholar
  115. Paul T, Tran TV, Elise P (2008) Vetiver systems applications: A technical reference. The Vetiver Network International, USGoogle Scholar
  116. Peremarti A, Bassie L, Christou P, Capell T (2009) Plant Mol Biol 70:253–264Google Scholar
  117. Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Plant Physiol 130:1454–1463Google Scholar
  118. Pillai MA, Akiyama T (2004) Mol Genet Genomics 271:141–149Google Scholar
  119. Ponappa T, Miller AR (1996) Physiol Plant 98:447–454Google Scholar
  120. Prabhavathi VR, Rajam MV (2007) Plant Biotech 24:273–282Google Scholar
  121. Rácz I, Kovács M, Lasztity D, Veisz O, Szalai G, Páldi E (1996) J Plant Physiol 148:368–373Google Scholar
  122. Rastogi R, Davies PJ (1991) In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants CRC Press, Boca Raton, FL pp 187–199Google Scholar
  123. Rea G, De Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, De Gara L, Federico R, Angelini R, Tavladoraki P (2004) Plant Physiol 134:1414–1426Google Scholar
  124. Reggiani R, Zaina S, Bertani A (1992) Phytochem 31:417–419Google Scholar
  125. Reggiani R, Bozob P, Bertania A (1994) Plant Sci 102:121–126Google Scholar
  126. Rodríguez AA, Grunberg KA, Taleisnik EL (2002) Plant Physiol 129:1627–1632Google Scholar
  127. Rodríguez AA, Córdoba AR, Ortega L, Taleisnik E (2004) J Exp Bot 55:1383–1390Google Scholar
  128. Rodríguez AA, Lascano R, Bustos D, Taleisnik E (2007) J Plant Physiol 164:223–230Google Scholar
  129. Rodríguez AA, Maiale SJ, Menéndez AB, Ruiz OA (2009) J Exp Bot 60:4249–4262Google Scholar
  130. Rodríguez-Kessler M, Alpuche-Solís AG, Ruiz OA, Jiménez-Bremont JF (2006) Plant Growth Reg 48:175–185Google Scholar
  131. Roy M, Wu R (2001) Plant Sci 160:869–875Google Scholar
  132. Roy M, Wu R (2002) Plant Sci 163:987–992Google Scholar
  133. Roy P, Niyogi K, Sengupta DN, Ghosh B (2005) Plant Sci 168:583–591Google Scholar
  134. Roychoudhury A, Basu S, Sarkar SN, Sengupta DN (2008) Plant Cell Rep 27:1395–1410Google Scholar
  135. Sebela M, Radova A, Angelini R, Tavladoraki P, Frebort II, Pec P (2001) Plant Sci 160:197–207Google Scholar
  136. Serrano S, Martínez-Madrid MC, Riquelme F, Romojaro F (1995) Physiol Plant 95:73–76Google Scholar
  137. Shabala S, Cuin TA, Pottosin I (2007) FEBS Lett 581:1993–1999Google Scholar
  138. Shen W, Nada K, Tachibana S (2000) Plant Physiol 124:431–439Google Scholar
  139. Shi IE, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Tree Physiol 30:914–922Google Scholar
  140. Shiozaki S, Ogata T, Horiuchi S (2000) Sci Hort 83:33–41Google Scholar
  141. Slocum RD (1991) Polyamine biosynthesis in plants. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants,. CRS Press, Boca Raton, FL, pp 23–40Google Scholar
  142. Srivastava SK, Rajbabu P (1983) Phytochem 22:2675–2679Google Scholar
  143. Sugiyama S, Vassylyev DG, Matsushima M, Kashiwagi K, Igarashi K, Morikawa K (1996) J Biol Chem 271:9519–9525Google Scholar
  144. Szalai G, Janda T, Bartók T, Páidi E (1997) Physiol Plant 101:434–438Google Scholar
  145. Szalai G, Pap M, Janda T (2009) J Plant Physiol 166:1826–1831Google Scholar
  146. Sziderics AH, Oufir M, Trognitz F, Kopecky D, Matušíková I, Hausman JF, Wilhelm, E (2010) Plant Cell Rep 29:295–305Google Scholar
  147. Takahashi T, Kakehi JI (2010) Ann Bot 105:1–6Google Scholar
  148. Tang W, Newton RJ, Li C Charles TM (2007) Plant Cell Rep 26:115–124Google Scholar
  149. Tassoni A, Antognoni FA, Bagni N (1996) Plant Physiol 110:817–824Google Scholar
  150. Tassoni A, Van Buuren M, Franceschetti M, Fornalè S, Bagni N (2000) Plant Physiol Biochem 38:383–393Google Scholar
  151. Tassoni A, Napier RM, Francescheti M, Venis MA, Bagni N (2002) Plant Physiol 128:1303–1312Google Scholar
  152. Tassoni A, Fornalè S, Bagni N (2003) Plant Physiol Biochem 41:871–875Google Scholar
  153. Theiss C, Bohley P, Voigt J (2002) Plant Physiol 128:1470–1479Google Scholar
  154. Tian A, Zhao J, Zhang J, Gai J, Chen S (2004) Theor Appl Genet 108:842–850Google Scholar
  155. Tiburcio AF, Besford RT, Capell T, Borrell A, Testillano PS, Risueno MC (1994) J Exp Bot 45:1789–1800Google Scholar
  156. Torrigiani P, Serafini-Fracassini D, Biondi S, Bagni N (1986) J Plant Physiol 124:23–29Google Scholar
  157. Toumi I, Moschou PN, Paschalidis KA, Bouamama B, Ben Salem-Fnayou A, Ghorbel AW, Mliki A, Roubelakis-Angelakis KA (2010) J Plant Physiol 167:519–525Google Scholar
  158. Turner LB, Stewart GR (1986) J Exp Bot 37:170–177Google Scholar
  159. Vassylyev DG, Tomitori H, Kashiwagi K, Morikawa K, Igarashi K (1998) J Biol Chem 273:17604–17609Google Scholar
  160. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J (2010) Plant Physiol BiochemGoogle Scholar
  161. Votyakova TV, Wallace HM, Dunbar B, Wilson SB (1999) Eur J Biochem 260:250–257Google Scholar
  162. Waie B, Rajam MV (2003) Plant Sci 164:727–734Google Scholar
  163. Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ, Honda C, Moriguchi T (2008) Transgenic Res 17:251–263Google Scholar
  164. Wi SJ, Kim WT, Park KY (2006) Plant Cell Rep 25:1111–1121Google Scholar
  165. Xing SG, Jun YB, Hau ZW, Liang LY (2007) Plant Physiol Biochem 45:560–566Google Scholar
  166. Yang J, Zhang J, Liu K, Wang Z, Liu L (2007) J Exp Bot 58:1545–1555Google Scholar
  167. Yin C, Duan B, Wang X, Li C (2004) Plant Sci 167:1091–1097Google Scholar
  168. Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J (2009) Sci Hortic 122:200–208Google Scholar
  169. Zhang X, Zang R, Li C (2004) Plant Sci 166:791–797Google Scholar
  170. Zhao FG, Qin P (2004) Plant Growth Reg 42:97–103Google Scholar
  171. Zheng YY, Hu J, Xu SC, Guan YJ, Wang XJ (2009) Seed Sci Tech 37:59–69Google Scholar
  172. Zhou Q, Yu B (2010) Plant Physiol Biochem 48:417–425Google Scholar
  173. Zhuang YL, Ren GJ, Zhu Y, Hou GH, Qu X, Li ZX, Yue GD, Zhang JR (2008) Physiologia Plantarum 52:759–762Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Ana Bernardina Menéndez
    • 1
  • Andrés Alberto Rodriguez
    • 1
  • Santiago Javier Maiale
    • 1
  • Kessler Margarita Rodriguez
    • 2
  • Bremont Juan Francisco Jimenez
    • 2
  • Oscar Adolfo Ruiz
    • 1
    Email author
  1. 1.Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús, Consejo Nacional de Investigaciones Científicas y TécnicasUniversidad de Buenos AiresChascomús, Prov. de Buenos AiresArgentina
  2. 2.Instituto Potosino de InvestigaciónCientífica y TecnológicaSan Luis PotosíMéxico

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