Abiotic Stress Resistance

  • Angela Roberta Lo PieroEmail author
Part of the Compendium of Plant Genomes book series (CPG)


Citrus, one of the most important fruit crops in the world, is sensitive to many environmental stresses often leading to poor tree growth and reductions in fruit yield and quality. Citrus is most often grown in warm climates with well-drained soils, therefore acceptable growth conditions depend upon the quality and quantity of irrigation water and the risk of cold temperatures. Citrus species do not develop a powerful root system and in well-drained soils of subtropical semiarid zones might be subjected to water deficit especially during hot dry summers. Then, these areas often require supplemental irrigation that may prompt the use of low quality water thereby increasing soil’s salt concentration. Even when irrigation water is of good quality, the use of fertilizers and other agro-chemicals raises the likelihood of salts to rise in the soil causing salinity stress, especially high chloride, which in turn is rather detrimental to citrus growth and fruit quality and yield. Negative soil characteristics such as excess calcium, high pH and mineral imbalances also affect citrus fruiting. In calcareous soils, for example, the high pH causes Fe-immobilization in unavailable forms for plant absorption thus causing iron deficiency. In addition, in areas characterized by scarcely drained soil, flooding can affect the soil structure depleting O2 for the radical tissues and provoking a reduction in iron solubility. Moreover, these damaging stresses do not come alone but in combination, in some cases acting according to an additive effect thus leading to a more restricted plant development. In this chapter, citrus plant behavior under the main abiotic stress conditions, such as drought, salinity and low temperatures will be deeply described, taking into account that important differences among genotypes have been described in their response. The effect of heat, flooding and heavy metal stresses will be also considered although the reader can refer to the existing literature to examine in depth these abiotic stresses. In conclusion, the consequences of the combined effect of more than one stress type at once, occurrence that normally mimics the natural environmental conditions, will be also reviewed.


  1. Aksoy A, Sahin U, Duman, F (2000) Robinia pseudo-acacia L. as a possible biomonitor of heavy metal pollution in Kayseri. Tr J Bot 24:279–284Google Scholar
  2. Allario T, Brumós J, Colmenero-Flores JM, Tadeo F, Froelicher Y, Talon M, Navarro L, Ollitrault P, Morillon R (2011) Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J Exp Bot 62:2507–2519PubMedPubMedCentralCrossRefGoogle Scholar
  3. Allario T, Brumós J, Colmenero-Flores JM, Iglesias DJ, Pina JA, Navarro L, Talon M, Ollitrault P, Morillon R (2013) Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environ 36:856–868PubMedCrossRefGoogle Scholar
  4. Alvarez-Gerding X, Cortés-Bullemore R, Medina C, Romero-Romero JL, Inostroza-Blancheteau C, Aquea F, Arce-Johnson P (2015) Improved salinity tolerance in Carrizo Citrange rootstock through overexpression of glyoxalase system genes. BioMed Res Int (art no 827951)Google Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  6. Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466PubMedCrossRefGoogle Scholar
  7. Bañuls J, Primo-Millo E (1992) Effects of chloride and sodium on gas exchange parameters and water relations of citrus plants. Physiol Plant 86:115–123CrossRefGoogle Scholar
  8. Bañuls J, Primo-Millo E (1995) Effects of salinity on some citrus scion–rootstock combinations. Ann Bot 76:97–102CrossRefGoogle Scholar
  9. Barrett HC (1992) An autotetraploid of the ‘Key Lime’ Citrus aurantifolia. Fruit Var J 46:66–170Google Scholar
  10. Brumós J, Colmenero-Flores J, Conesa A, Izquierdo P, Sánchez G, Iglesias D, López-Climent M, Gómez-Cadenas A, Talón M (2009) Membrane transporters and carbon metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and sensitive citrus rootstocks. Funct Integr Genomics 9:293–309PubMedCrossRefGoogle Scholar
  11. Cai Y, Cao F, Cheng W, Zhang G, Wu F (2011) Modulation of exogenous glutathione in phytochelatins and photosynthetic performance against Cd stress in the two rice genotypes differing in Cd tolerance. Biol Trace Elem Res 143:1159–1173PubMedCrossRefGoogle Scholar
  12. Cameron JW, Soost RK (1968) Characters of new populations of citrus polyploids, and the relation between tetraploidy in the pollen parent and hybrid tetraploid progeny. In: 1st international citrus symposium, Riverside, pp 199–205Google Scholar
  13. Cataldo DA, Wildung RE (1978) Soil and plant factors influencing the accumulation of heavy metals by plants. Environ Health Persp 27:149–159CrossRefGoogle Scholar
  14. Chehregani A, Malayeri BE (2007) Removal of heavy metals by native accumulator plants. Int J Agric Biol 9:462–465Google Scholar
  15. Chica EJ, Albrigo LG (2013) Expression of flower promoting genes in sweet orange during floral inductive water deficits. J Am Soc Hortic Sci 138:88–94CrossRefGoogle Scholar
  16. Chinnusamy V, Zhu J, Zhu J (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451CrossRefGoogle Scholar
  17. Clarke SM, Mur LAJ, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermos tolerance in Arabidopsis thaliana. Plant J 38:432–447PubMedCrossRefGoogle Scholar
  18. Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315PubMedCrossRefGoogle Scholar
  19. Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumós J, Talon M (2007) Identification and functional characterization of cation–chloride cotransporters in plants. Plant J 50:278–292PubMedCrossRefGoogle Scholar
  20. Cope RB (2004) Helping animals exposed to the herbicide paraquat. Vet Med 99:755–762Google Scholar
  21. Crifò T, Puglisi I, Petrone G, Reforgiato Reforgiato G, Lo Piero AR (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476:1–9CrossRefGoogle Scholar
  22. Crifò T, Petrone G, Lo Cicero L, Lo Piero AR (2012) Short cold storage enhances the anthocyanin contents and level of transcripts related to their biosynthesis in blood oranges. J Agric Food Chem 60:476–481CrossRefGoogle Scholar
  23. Dahro B, Wang F, Peng T, Liu JH (2016) PtrA/NINV, an alkaline/neutral invertase gene of Poncirus trifoliata, confers enhanced tolerance to multiple abiotic stresses by modulating ROS levels and maintaining photosynthetic efficiency. BMC Plant Biol 16(art no 76)Google Scholar
  24. Danquah A, Zelicourt DA, Colcombet J, Hirt H (2013) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52PubMedCrossRefGoogle Scholar
  25. Davenport TL (1990) Citrus flowering. Hortic Rev 12:349–408Google Scholar
  26. Davies FS, Albrigo LG (1994) Citrus. Cab International, Wallingford, UKGoogle Scholar
  27. de Campos MKF, de Carvalho K, de Souza FS, Marur CJ, Pereira LFP, Filho JCB, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic ‘Swingle’ citrumelo plants over-accumulating proline. Environ Exp Bot 72:242–250CrossRefGoogle Scholar
  28. De Paula Santos Martins C, Neves DM, Cidade LC, Mendes AFS, Silva DC, Almeida AF, Coelho-Filho MA, Gesteira AS, Soares-Filho WS, Costa MGC (2017) Expression of the citrus CsTIP2;1 gene improves tobacco plant growth, antioxidant capacity and physiological adaptation under stress conditions. Planta 245:951–963PubMedCrossRefGoogle Scholar
  29. De Paula Santos Martins C, Pedrosa AM, Du D, Gonçalves LP, Yu Q, Gmitter FG, Costa MGC (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS One 10(art no e0138786)Google Scholar
  30. De Souza JD, De Andrade Silva EM, Filho MAC, Morillon R, Bonatto D, Micheli F, Da Silva Gesteira (2017) A different adaptation strategies of two citrus scion/rootstock combinations in response to drought stress. PLoS One 12(art no e0177993)Google Scholar
  31. Distefano G, Gentile A, Hedhly A, La Malfa S (2018) Temperatures during flower bud development affect pollen germination, self-incompatibility reaction and early fruit development of clementine (Citrus clementina Hort. ex Tan.). Plant Biol 20:191–198PubMedCrossRefGoogle Scholar
  32. Doganlar ZB, Atmaca M (2011) Influence of airborne pollution on Cd, Zn, Pb, Cu, and Al accumulation and physiological parameters of plant leaves in Antakya (Turkey). Water Air Soil Poll 214:509–523CrossRefGoogle Scholar
  33. Doganlar ZB, Yurekli F (2009) Interactions between cadmium and phytochelatin accumulation in two different sunflower cultivars. Fresen Environ Bull 18:304–310Google Scholar
  34. Ebel RC, Nesbitt ML, Dozier WA, Dane F (2008) Freeze risk and protection measures of Satsuma mandarins grown in the southeastern United States. HortScience 43:87–289Google Scholar
  35. Fernández-Ballester G, García-Sánchez F, Cerdá A, Martínez V (2003) Tolerance of citrus rootstock seedlings to saline stress based on their ability to regulate ion uptake and transport. Tree Physiol 23:265–271PubMedCrossRefGoogle Scholar
  36. Fernández-Crespo E, Gómez-Pastor R, Scalschi L, Llorens E, Camañes G, García-Agustín P (2014) NH4+ induces antioxidant cellular machinery and provides resistance to salt stress in citrus plants. Trees-Struct Funct 28:1693–1704CrossRefGoogle Scholar
  37. Fu XZ, Khan EU, Hu, SS, Fan QJ Liu JH (2011) Overexpression of the betaine aldehyde dehydrogenase gene from Atriplex hortensis enhances salt tolerance in the transgenic trifoliate orange (Poncirus trifoliata L. Raf.). Environ Exp Bot 74:106–113CrossRefGoogle Scholar
  38. Fu XZ, Huang Y, Xing F, Chun CP, Ling LL, Cao L, Peng LZ (2016) Changes in free polyamines and expression of polyamine metabolic genes under drought and high-temperature in Citrus sinensis. Biol Plant 60:793–798CrossRefGoogle Scholar
  39. Fu XZ, Tong YH, Zhou X, Ling LL, Chun CP, Cao L, Zeng M, Peng LZ (2017) Genome-wide identification of sweet orange (Citrus sinensis) metal tolerance proteins and analysis of their expression patterns under zinc, manganese, copper, and cadmium toxicity. Gene 629:1–8PubMedCrossRefGoogle Scholar
  40. Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot 59: 2393–2402PubMedPubMedCentralCrossRefGoogle Scholar
  41. Garcia-Sanchez F, Syvertsen JP (2006) Salinity tolerance of Cleopatra mandarin and Carrizo citrange citrus rootstock seedling is affected by CO2 enrichment during growth. J Am Soc Hortic Sci 131:24–31Google Scholar
  42. Garcia-Sanchez F, Rubio F, Martinez V (2010) Abiotic stresses: salinity and drought. In: Gonzalez-Fontes A, Garate A, Bonilla I (eds) Agricultural sciences: topics in modern agriculture. Studium Press, USA, pp 1–545Google Scholar
  43. García‐Sánchez F, Syvertsen JP, Gimeno V, Botía P, Perez‐Perez JP (2007) Responses to flooding and drought stress by two citrus rootstock seedlings with different water‐use efficiency Physiol Plantarum 130:532–542CrossRefGoogle Scholar
  44. Geng J, Liu JH (2018) The transcription factor CsbHLH18 of sweet orange functions in modulation of cold tolerance and homeostasis of reactive oxygen species by regulating the antioxidant gene. J Exp Bot 69:2677–2692PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442PubMedCrossRefGoogle Scholar
  46. Gimeno V, Syvertsen JP, Nieves M, Simon I, Martínez V, Garcia-Sanchez F (2009) Additional nitrogen fertilization affects salt tolerance of lemon trees on different rootstocks. Sci Hortic 121:298–305CrossRefGoogle Scholar
  47. Gmitter FG Jr (1994) Contemporary approaches to improving citrus cultivars. HortTechnology 4:206–210CrossRefGoogle Scholar
  48. Gonçalves LP, Alves TFO, Martins CPS, de Sousa AO, dos Santos IC, Pirovani CP, Almeida AAF, Filho MAC, Gesteira AS, Soares Filho WS, Girardi EA, Costa MGC (2016) Rootstock-induced physiological and biochemical mechanisms of drought tolerance in sweet orange. Acta Physiol Plant 38(art no 174)Google Scholar
  49. Gong XQ, Liu JH (2013) Genetic transformation and genes for resistance to abiotic and biotic stresses in Citrus and its related genera. Plant Cell Tissue Org 113:137–147CrossRefGoogle Scholar
  50. Gong X, Zhang J, Hu J, Wang W, Wu H, Zhang Q, Liu JH (2015) FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ 38:2248–2262CrossRefGoogle Scholar
  51. Grattan SR, Grieve CM (1992) Mineral element acquisition and growth response of plants grown in saline environments. Agric Ecosyst Environ 38:275–300CrossRefGoogle Scholar
  52. Grieve AM, Prior LD, Bevington KB (2007) Long-term effects of saline irrigation water on growth, yield, and fruit quality of Valencia orange trees. Aust J Agric Res 58:342–348Google Scholar
  53. Grosser JW, Gmitter FG Jr (1990) Protoplast fusion and citrus improvement. Plant Breed Rev 8:339–374Google Scholar
  54. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11PubMedCrossRefGoogle Scholar
  55. Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703PubMedCrossRefGoogle Scholar
  56. Haynes RJ, Swift RS (1985) Effects of air-drying on the adsorption and desorption of phosphate and levels of extractable phosphate in a group of acid soils New Zealand. Geoderma 35:145–157CrossRefGoogle Scholar
  57. He LG, Wang HL, Liu DC, Zhao YJ, Xu M, Zhu M, Sunday ZH (2012) Isolation and expression of a cold-responsive gene PtCBF in Poncirus trifoliata and isolation of citrus CBF promoters. Biol Plant 56:484–492CrossRefGoogle Scholar
  58. Huang X, Zhang Q, Zhu D, Fu X,Wang M, Zhang Q. Moriguchi T, Liu J (2015) ICE1 of Poncirus trifoliata functions in cold tolerance by modulating polyamine levels through interacting with arginine decarboxylase. J Exp Bot 66:3259–3274PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hussain S, Curk F, Dhuique-Mayer C, Urban L, Ollitrault P, Luro F, Morillond R (2012) Autotetraploid trifoliate orange (Poncirus trifoliata) rootstocks do not impact clementine quality but reduce fruit yields and highly modify rootstock/scion physiology. Sci Hortic 134:100–107CrossRefGoogle Scholar
  60. Hussain S, Morillon R, Anjum MA, Ollitrault P, Costantino G, Luro F (2015) Genetic diversity revealed by physiological behavior of citrus genotypes subjected to salt stress. Acta Physiol Plant 37(art no 1740)Google Scholar
  61. Inch S, Stover E, Driggers R, Lee RF (2014) Freeze response of citrus and citrus-related genotypes in a Florida field planting. HortScience 49:1010–1016CrossRefGoogle Scholar
  62. IPCC (2014) Summary of policymakers of the synthesis report.
  63. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy, F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111PubMedCrossRefGoogle Scholar
  64. Kıran Y, Sahin A (2005) The effects of the lead on the seed germination, root growth, and root tip cell mitotic divisions of Lens culinaris Medik. Gazi Univ J Sci 18:17–25Google Scholar
  65. Krajewski AJ, Rabe E (1995) Bud age affects sprouting and flowering in Clementine mandarin (Citrus reticulata Blanco). HortScience 30:1366–1368CrossRefGoogle Scholar
  66. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. San Diego, Academic PressGoogle Scholar
  67. Lafuente MT, Establés-Ortíz B, González-Candelas L (2017) Insights into the molecular events that regulate heat-induced chilling tolerance in citrus fruits. Front Plant Sci 8(art no 1113)Google Scholar
  68. Lang P, Zhang C, Ebel RC, Dane F, Dozier WA (2005) Identification of cold acclimated genes in leaves of Citrus unshiu by mRNA differential display. Gene 359:111–118PubMedPubMedCentralCrossRefGoogle Scholar
  69. Levy Y, Syvertsen JP (2004) Irrigation water quality and salinity effects in citrus trees. Hortic Rev 30:37–82Google Scholar
  70. Li JX, Hou XJ, Zhu J, Zhou JJ, Huang HB, Yue JQ, Gao JY, Du YX, Hu CX, Hu CG, Zhang JZ (2017) Identification of genes associated with lemon floral transition and flower development during floral inductive water deficits: a hypothetical model. Front Plant Sci 8(art no 1013)Google Scholar
  71. Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599PubMedCrossRefGoogle Scholar
  72. Liu J, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6(art no 827)Google Scholar
  73. Lo Cicero L, Madesis P, Tsaftaris A, Lo Piero AR (2015) Tobacco plants over-expressing the sweet orange tau glutathione transferases (CsGSTUs) acquire tolerance to the diphenyl ether herbicide fluorodifen and to salt and drought stresses. Phytochemistry 116:69–77PubMedCrossRefGoogle Scholar
  74. Lo Cicero L, Catara V, Strano CP, Bella P, Madesis P, Lo Piero AR (2017) Over-expression of Cs GSTUs promotes tolerance to the chloroacetanilide herbicide alachlor and resistance to Pseudomonas Syringae pv. tabaci in transgenic tobacco. Biol Plant 61:160–177Google Scholar
  75. Lo Piero AR (2015) The state of art on biosynthesis of anthocyanins and its regulation in pigmented sweet oranges [(Citrus sinensis) L. Osbeck]. J Agric Food Chem 63:4031–4041PubMedCrossRefGoogle Scholar
  76. Lo Piero AR, Puglisi I, Rapisarda P, Petrone G (2005) Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. J Agric Food Chem 53:9083–9088CrossRefGoogle Scholar
  77. Lo Piero AR, Puglisi I, Petrone G (2006) Gene isolation, analysis of expression and in vitro synthesis of a glutathione S-transferase from orange fruit. [Citrus sinensis L. (Osbeck)]. J Agric Food Chem 54:9227–9233Google Scholar
  78. Lo Piero AR, Mercurio V, Puglisi I, Petrone G (2009) Gene isolation and expression analysis of two distinct sweet orange [(Citrus sinensis) L. (Osbeck)] tau-type glutathione transferase. Gene 443:143–150PubMedCrossRefGoogle Scholar
  79. Lo Piero AR, Mercurio V, Puglisi I, Petrone G (2010) Different role of functional residues in the hydrophobic binding site of two sweet orange tau glutathione S-transferases. FEBS J 277:255–262PubMedCrossRefGoogle Scholar
  80. Lo Piero AR, Puglisi I, Mercurio V, Petrone G (2011) Engineering the xenobiotic substrate specificity of sweet orange tau glutathione S-transferase. Acta Hortic 892:143–147CrossRefGoogle Scholar
  81. Lo Piero AR, Lo Cicero L, Puglisi I (2014) The metabolic fate of citric acid as affected by cold storage in blood oranges. J Plant Biochem Biotech 23:161–166CrossRefGoogle Scholar
  82. Lόpez-Climent MF, Arbona V, Pérez-Clemente RM, Gόmez-Cadenas A (2011) Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plant 55:187–190CrossRefGoogle Scholar
  83. Lόpez-Climent MF, Arbona V, Pérez-Clemente RM, Zandalinas SI, Gόmez-Cadenas A (2014) A effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biol 16:79–87CrossRefGoogle Scholar
  84. Maas EV (1986) Salt tolerance in plants. Appl Plant Sci 1:12–26Google Scholar
  85. Maas EV (1993) Salinity and citriculture. Tree Physiol 12:195–216PubMedCrossRefGoogle Scholar
  86. Marschner H (1995) Mineral nutrition in higher plants, 2nd edn. Academic Press, London, UKGoogle Scholar
  87. Martínez-Alcántara B, Martínez-Cuenca MR, Quiñones A, Iglesias DJ, Primo-Millo E, Forner-Giner MA (2015) Comparative expression of candidate genes involved in sodium transport and compartmentation in citrus. Environ Exp Bot 111:52–62CrossRefGoogle Scholar
  88. Martínez-Cuenca MR, Quiñones A, Primo-Millo E, Forner-Giner MA (2015) Flooding impairs Fe uptake and distribution in Citrus due to the strong down-regulation of genes involved in strategy I responses to Fe deficiency in roots PLoS One 10(art no e0123644)Google Scholar
  89. Maul P, McCollum GT, Popp M, Guy CL, Porat R (2008) Transcriptome profiling of grapefruit flavedo following exposure to low temperature and conditioning treatments uncovers principal molecular components involved in chilling tolerance and susceptibility. Plant Cell Environ 31:752–768PubMedCrossRefGoogle Scholar
  90. Molinari HBC, Marur CJ, Filho JCB, Kobayashi AK, Pileggi M, Junior RPL, Pereira LFP, Vieira LGE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. X Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381CrossRefGoogle Scholar
  91. Moreno P, Ambrós S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Mol Plant Pathol 9:251–268PubMedPubMedCentralCrossRefGoogle Scholar
  92. Moya JL, Tadeo FR, Gomez-Cadenas A, Primo-Millo E, Talon M (2002) Transmissible salt tolerance traits identified through reciprocal grafts between sensitive Carrizo and tolerant Cleopatra citrus genotypes. J Plant Physiol 159:991–998CrossRefGoogle Scholar
  93. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedPubMedCentralCrossRefGoogle Scholar
  94. Neves DM, Almeida LADH, Santana-Vieira DDS, Freschi L, Ferreira CF, Soares Filho WDS, Costa MGC, Micheli F, Coelho Filho M, Gesteira ADS (2017) Recurrent water deficit causes epigenetic and hormonal changes in citrus plants. Sci Rep 7(art no 13684)Google Scholar
  95. Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, Omura M, Ikoma Y (2007) Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J Exp Bot 58:3915–3927PubMedCrossRefGoogle Scholar
  96. Oustric J, Morillon R, Ollitrault P, Herbette S, Luro F, Froelicher Y, Tur I, Dambier D, Giannettini J, Berti L, Santini J (2018) Somatic hybridization between diploid Poncirus and Citrus improves natural chilling and light stress tolerances compared with equivalent doubled-diploid genotypes. Trees Struct Func 32:883–895CrossRefGoogle Scholar
  97. Ouzounidou G (1994) Copper-induced changes on growth metal content and photosynthetic function of Alyssum montanum L. plants. Environ Exp Bot 34:165–172CrossRefGoogle Scholar
  98. Pannitteri C, Continella A, Lo Cicero L, Gentile A, La Malfa S, Sperlinga E, Napoli EM, Strano T, Ruberto G, Siracusa L (2017) Influence of postharvest treatments on qualitative and chemical parameters of Tarocco blood orange fruits to be used for fresh chilled juice. Food Chem 230:441–447PubMedCrossRefGoogle Scholar
  99. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedPubMedCentralCrossRefGoogle Scholar
  100. Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628PubMedCrossRefGoogle Scholar
  101. Peng T, Zhu X, Duan N, Liu JH (2014) PtrBAM1, a β-amylase-coding gene of Poncirus trifoliata, is a CBF regulon member with function in cold tolerance by modulating soluble sugar levels. Plant Cell Environ 37:2754–2767CrossRefGoogle Scholar
  102. Peralta-Videa JR, de la Rosa G, Gonzalez JH, Gardea-Torresdey JL (2004) Effects of the growth stage on the heavy metal tolerance of alfalfa plants. Adv Environ Res 8:679–685CrossRefGoogle Scholar
  103. Peréz-Peréz JG, Romero P, Navarro JM, Botia P (2008) Response of sweet orange cv ‘lane late’ to deficit irrigation in two rootstocks. I: water relations, leaf gas exchange and vegetative growth. Irrig Sci 26:415–425CrossRefGoogle Scholar
  104. Perotti VE, Moreno AS, Trípodi KEJ, Meier G, Bello F, Cocco M, Vázquez D, Anderson C, Podestá FE (2015) Proteomic and metabolomic profiling of Valencia orange fruit after natural frost exposure. Physiol Plant 153:337–354PubMedCrossRefGoogle Scholar
  105. Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312CrossRefGoogle Scholar
  106. Pizzio GA, Rodriguez L, Antoni R, Gonzalez-Guzman M, Yunta C, Merilo E, Kollist H, Albert A, Rodriguez PL (2013) The PYL4 A194T mutant uncovers a key role of PYL4-PP2CA interaction for ABA signaling and plant drought resistance. Plant Physiol 163:441–455Google Scholar
  107. Rodrigo MJ, Alquezar B, Zacarías L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643PubMedCrossRefGoogle Scholar
  108. Rodríguez-Gamir J, Ancillo G, Legaz F, Primo-Millo E, Forner-Giner MA (2012) Influence of salinity on pip gene expression in citrus roots and its relationship with root hydraulic conductance, transpiration and chloride exclusion from leaves. Environ Exp Bot 78:163–166CrossRefGoogle Scholar
  109. Romero P, Navarro JM, Pérez-Pérez J, García-Sánchez F, Gómez-Gómez A, Porras I, Martinez V, Botía P (2006) Deficit irrigation and rootstock: their effects on water relations, vegetative development, yield, fruit quality and mineral nutrition of Clemenules mandarin. Tree Physiol 26:1537–1548PubMedCrossRefGoogle Scholar
  110. Rose ML, Scwarzacher T, Heslop-Harrison JS (1998) The chromosomes of citrus and poncirus species and hybrids: identification of characteristic chromosomes and physical mapping of rDNA loci using in situ hybridization and fluorochrome banding. J Hered 89:83–86CrossRefGoogle Scholar
  111. Ruiz M, Quiñones A, Martínez-Alcántara,B, Aleza P, Morillon R, Navarro L, Primo-Millo E, Martínez-Cuenca MR (2016) Effects of salinity on diploid (2x) and doubled diploid (4x) Citrus macrophylla genotypes. Sci Hortic 207:33–40CrossRefGoogle Scholar
  112. Şahin-Çevik M (2013) Identification and expression analysis of early cold-induced genes from cold-hardy Citrus relative Poncirus trifoliata (L.). Raf Gene 512:536–545PubMedCrossRefGoogle Scholar
  113. Şahin-Çevik M, Moore GA (2006) Identification and expression analysis of cold-regulated genes from the cold-hardy Citrus relative Poncirus trifoliata (L.). Raf Plant Mol Biol 62:83–97PubMedCrossRefGoogle Scholar
  114. Şahin-Çevik M, Moore GA (2013) Identification of a drought- and cold-stress inducible WRKY gene in the cold-hardy Citrus relative Poncirus trifoliate. N Z J Crop Hortic Sci 41:57–68CrossRefGoogle Scholar
  115. Şahin-Çevik M, Çevik B, Aşkin MA (2013) An abiotic stress-responsive WRKY gene is transiently induced in response to cold and drought stresses in Poncirus trifoliate. J Plant Interact 8:242–254CrossRefGoogle Scholar
  116. Şahin-Çevik M, Çevik B, Topkaya-Kütük B, Yazıcı K (2017) Identification of drought-induced genes from the leaves of Rangpur lime (Citrus limon (L) Osbeck). J Hortic Sci Biotech 92:636–645CrossRefGoogle Scholar
  117. Saleh B, Allario T, Dambier D, Ollitrault P, Morillon R (2008) Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. C R Biol 331:703–710PubMedPubMedCentralCrossRefGoogle Scholar
  118. Sanchez-Ballesta MT, Lluch Y, Gosalbes MJ, Zacarias L, Granell A, Lafuente MT (2003) A survey of genes differentially expressed during long-term heat-induced chilling tolerance in citrus fruit. Planta 218:65–70PubMedCrossRefGoogle Scholar
  119. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014PubMedCrossRefGoogle Scholar
  120. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot (art 217037):1–26CrossRefGoogle Scholar
  121. Soost RK, Cameron JW (1975) Citrus. In: Janick J, Moore JN (eds) Advances in fruit breeding. Purdue University Press, West Lafayette, IN, pp 507–540Google Scholar
  122. Soost RK, Roose ML (1996) Citrus. In: Janick J, Moore JN (eds) Fruit breeding: tree and tropical fruits. Wiley, NY, pp 257–323Google Scholar
  123. Syvertsen JP, Garcia-Sanchez F (2014) Multiple abiotic stresses occurring with salinity stress in citrus. Environ Exp Bot 103:128–137CrossRefGoogle Scholar
  124. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefGoogle Scholar
  125. Tan FQ, Tu H, Liang WJ, Long JM, Wu XM, Zhang HY, Guo WW (2015) Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biol 15(art no 89)Google Scholar
  126. Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599PubMedCrossRefGoogle Scholar
  127. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8PubMedPubMedCentralCrossRefGoogle Scholar
  128. Walker RR (1986) Sodium exclusion and potassium-sodium selectivity in salt-treated trifoliate orange (Poncirus trifoliata) and Cleopatra mandarin (Citrus reticulata) plants. Aust J Plant Physiol 13:293–303Google Scholar
  129. Wang Y, Zhang H, Hou P, Su X, Zhao P, Zhao H, Liu S (2014) Foliar-applied salicylic acid alleviates heat and high light stress induced photoinhibition in wheat (Triticum aestivum) during the grain filling stage by modulating the psbA gene transcription and antioxidant defense. Plant Growth Regul 73:289–297CrossRefGoogle Scholar
  130. Wedding JB, Carlson RW, Stukel JJ, Bazzaz FA (1975) Aereosol deposition on plant leaves. Environ Sci Technol 9:151–153CrossRefGoogle Scholar
  131. Xian L, Sun P, Hu S, Wu J, Liu JH (2014) Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses. Planta 239:61–77PubMedCrossRefGoogle Scholar
  132. Xie R, Li Y, He S, Zheng Y, Yi S, Lv Q, Deng L (2014) Genome-wide analysis of citrus R2R3MYB genes and their spatiotemporal expression under stresses and hormone treatments. PLoS ONE 9(art no e113971)Google Scholar
  133. Xie R, Pan X, Zhang J, Ma Y, He S, Zheng Y, Ma Y (2018) Effect of salt-stress on gene expression in citrus roots revealed by RNA-seq. Funct Integr Genomics 18:155–173PubMedCrossRefGoogle Scholar
  134. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66CrossRefGoogle Scholar
  135. Yelenosky G (1985) Cold hardiness in citrus. Hortic Rev 7:201–238Google Scholar
  136. Zaher-Ara T, Boroomand N, Sadat-Hosseini M (2016) Physiological and morphological response to drought stress in seedlings of ten citrus. Trees Struct Funct 30:985–993CrossRefGoogle Scholar
  137. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A, Inupakutika MA, Mittler R (2016a) ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J Exp Bot 67: 5381–5390PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zandalinas SI, Rivero RM, Martínez V, Gómez-Cadenas A, Arbona V (2016b) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol 16:105–121Google Scholar
  139. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A (2017a) Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in citrus. Front Plant Sci 8(art no 953)Google Scholar
  140. Zandalinas SI, Sales C, Beltrán J, Gómez-Cadenas A, Arbona V (2017b) Activation of secondary metabolism in citrus plants is associated to sensitivity to combined drought and high temperatures. Front Plant Sci 7(art no 1954)Google Scholar
  141. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Regulation of citrus responses to the combined action of drought and high temperatures depends on the severity of water deprivation. Physiola Plant 162:427–438CrossRefGoogle Scholar
  142. Zhang J, Nguyen HT, Blum A (1999) Genetic analysis of osmotic adjustment in crop plants. J Exp Bot 50:291–302CrossRefGoogle Scholar
  143. Zhang CK, Lang P, Dane F, Ebel RC, Singh NK, Locy RD, Dozier WA (2005a) Cold acclimation induced genes of trifoliate orange (Poncirus trifoliata). Plant Cell Rep 23:764–769PubMedCrossRefGoogle Scholar
  144. Zhang CK, Lang P, Ebel RC, Dane F, Singh NK, Locy RD, Dozier WA (2005b) Cold acclimation down regulated genes in Poncirus trifoliata. Can J Plant Sci 85:417–424CrossRefGoogle Scholar
  145. Zhu A, Li W, Ye J, Sun X, Ding Y, Cheng Y, Deng X (2011) Microarray expression profiling of postharvest Ponkan Mandarin (Citrus reticulata) fruit under cold storage reveals regulatory gene candidates and implications on soluble sugars metabolism. J Integr Plant Biol 53:358–374PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Agriculture, Food and EnvironmentUniversity of CataniaCataniaItaly

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