, Volume 33, Issue 6, pp 1711–1722 | Cite as

Time course of physiological responses in kiwifruit induced by bicarbonate

  • Nannan Wang
  • Xueyi Jiao
  • Tianli Guo
  • Cuiying Li
  • Zhande Liu
  • Fengwang MaEmail author
Original Article


Key message

Ionic imbalance is one adaptive strategy of kiwifruit to bicarbonate, as indicated mainly by NH4+ accumulation and increased NH4+/NO3 in bicarbonate-treated roots as well as decreased NH4+/NO3 in bicarbonate-treated leaves.


Bicarbonate-induced leaf chlorosis is frequently observed in kiwifruit orchards. A time-course experiment was conducted to investigate the effects of bicarbonate stress on the growth, root acidification, and organic acid and nutrient concentrations of kiwifruit plants treated for 7, 14, 21, 28, and 42 days in hydroponics. After 21 days of bicarbonate treatment, the kiwifruit vines exhibited leaf chlorosis, as indicated by decreased SPAD, chlorophyll a and b as well as carotenoid. Moreover, bicarbonate treatment induced NH4+ accumulation and NO3 reduction in roots from day 21 onward, thereby increasing the ratio of NH4+ to NO3 in roots, and the opposite was true for leaves that seemed to respond to bicarbonate earlier than roots but in an inconsistent manner. Before leaf chlorosis, bicarbonate imposition induced succinic acid accumulation and K reduction in roots from day 14 onward. However, the K concentration increased in bicarbonate-treated leaves from day 28 onward. Bicarbonate treatment also reduced P in all plant parts and Fe in leaves from day 21 onward, lowered Zn and enhanced Ca and Mg in roots from day 28 onward. In addition, bicarbonate treatment increased citric acid and ferric chelate reductase (FCR) activity in roots at days 7 and 14, but decreased citric acid and H+ extrusion at day 28 and decreased FCR activity at day 42, respectively, indicating that root acidification is duration dependent. These results suggest that, except for succinic acid accumulation, ionic imbalance in the whole kiwifruit plants (particularly N form’s shift) might be an alternative strategy to adapt to bicarbonate stress.


Bicarbonate stress Actinidia Ionic imbalance Nitrogen forms Succinic acid 



This work was funded by the National Natural Science Foundation of China (31601710), the Affiliated Foundation for Shaanxi Postdoctors of the National Natural Science Foundation of China (K3380218082), and the Scientific Startup Foundation for Doctors of Northwest A and F University (Z109021611).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Alcántara E, Montilla I, Ramírez P, García-Molina P, Romera FJ (2012) Evaluation of quince clones for tolerance to iron chlorosis on calcareous soil under field conditions. Sci Hortic 138:50–54. CrossRefGoogle Scholar
  2. Alhendawi R, Römheld V, Kirkby E, Marschner H (1997) Influence of increasing bicarbonate concentrations on plant growth, organic acid accumulation in roots and iron uptake by barley, sorghum, and maize. J Plant Nutr 20:1731–1753. CrossRefGoogle Scholar
  3. Ariz I, Artola E, Asensio AC, Cruchaga S, Aparicio-Tejo PM, Moran JF (2011) High irradiance increases NH4 + tolerance in Pisum sativum: higher carbon and energy availability improve ion balance but not N assimilation. J Plant Physiol 168:1009–1015. CrossRefPubMedGoogle Scholar
  4. Assimakopoulou A, Holevas CD, Fasseas K (2011) Relative susceptibility of some Prunus rootstocks in hydroponics to iron deficiency. J Plant Nutr 34:1014–1033. CrossRefGoogle Scholar
  5. Assimakopoulou A, Nifakos K, Kalogeropoulos P, Salmas I, Agelopoulos K (2016) Response of ungrafted rootstocks and rootstocks grafted with wine grape varieties (Vitis sp.) to ‘lime-induced chlorosis’. J Plant Nutr 39:71–86. CrossRefGoogle Scholar
  6. Bao SD (2000) Soil agro-chemistrical analysis, 2nd edn. China Agriculture Press, BeijingGoogle Scholar
  7. Bavaresco L, Poni S (2003) Effect of calcareous soil on photosynthesis rate, mineral nutrition, and source-sink ratio of table grape. J Plant Nutr 26:2123–2135. CrossRefGoogle Scholar
  8. Bittsánszky A, Pilinszky K, Gyulai G, Komives T (2015) Overcoming ammonium toxicity. Plant Sci 231:184–190. CrossRefPubMedGoogle Scholar
  9. Brautigam A, Gagneul D, Weber AP (2007) High-throughput colorimetric method for the parallel assay of glyoxylic acid and ammonium in a single extract. Anal Biochem 362:151–153. CrossRefPubMedGoogle Scholar
  10. Cambrollé J, García JL, Ocete R, Figueroa ME, Cantos M (2015) Evaluating tolerance to calcareous soils in Vitis vinifera ssp. Sylvestris. Plant Soil 396:1–11. CrossRefGoogle Scholar
  11. Chen HF, Zhang Q, Cai HM, Zhou W, Xu FS (2018) H2O2 mediates nitrate-induced iron chlorosis by regulating iron homeostasis in rice. Plant Cell Environ 41:767–781. CrossRefPubMedGoogle Scholar
  12. Chouliaras V, Dimassi K, Therios I, Molassiotis A, Diamantidis G (2004a) Root-reducing capacity, rhizosphere acidification, peroxidase and catalase activities and nutrient levels of Citrus taiwanica and C. volkameriana seedlings, under Fe deprivation conditions. Agron 24:1–6. CrossRefGoogle Scholar
  13. Chouliaras V, Therios I, Molassiotis A, Dimantidis G (2004b) Iron chlorosis in grafted sweet orange (Citrus sinensis L.) plants: physiological and biochemical responses. Biol Plant 48:141–144. CrossRefGoogle Scholar
  14. Coskun D, Britto DT, Kronzucker HJ (2017) The nitrogen-potassium intersection: membranes, metabolism, and mechanism. Plant Cell Environ 40:2029–2041. CrossRefPubMedGoogle Scholar
  15. Covarrubias JI, Rombolà AD (2013) Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate. Plant Soil 370:305–315. CrossRefGoogle Scholar
  16. Covarrubias JI, Rombolà AD (2015) Organic acids metabolism in roots of grapevine rootstocks under severe iron deficiency. Plant Soil 394:165–175. CrossRefGoogle Scholar
  17. Covarrubias JI, Pisi A, Rombolà AD (2014) Evaluation of sustainable management techniques for preventing iron chlorosis in the grapevine. Aust J Grape Wine Res 20:149–159. CrossRefGoogle Scholar
  18. Covarrubias JI, Retamales C, Donnini S, Rombolà AD, Pastenes C (2016) Contrasting physiological responses to iron deficiency in Cabernet Sauvignon grapevines grafted on two rootstocks. Sci Hortic 199:1–8. CrossRefGoogle Scholar
  19. Curie C, Mari S (2017) New routes for plant iron mining. New Phytol 214:521–525. CrossRefPubMedGoogle Scholar
  20. De Nisi P, Zocchi G (2000) Phosphoenolpyruvate carboxylase in cucumber (Cucumis sativus L.) roots under iron deficiency: activity and kinetic characterization. J Exp Bot 352:1903–1909. CrossRefGoogle Scholar
  21. Demasi S, Caser M, Handa T, Kobayashi N, Pascale SD, Scariot V (2017) Adaptation to iron deficiency and high pH in evergreen azaleas (Rhododendron spp.): potential resources for breeding. Euphytica. CrossRefGoogle Scholar
  22. Ding W, Clode PL, Lambers H (2019) Effects of pH and bicarbonate on the nutrient status and growth of three Lupinus species. Plant Soil. CrossRefGoogle Scholar
  23. Donnini S, Castagna A, Ranieri A, Zocchi G (2009) Differential responses in pear and quince genotypes induced by Fe deficiency and bicarbonate. J Plant Physiol 166:1181–1193. CrossRefPubMedGoogle Scholar
  24. Donnini S, De Nisi P, Gabotti D, Tato L, Zocchi G (2012) Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability. Plant Cell Environ 35:1171–1184. CrossRefPubMedGoogle Scholar
  25. Esteban R, Ariz I, Cruz C, Moran JF (2016) Review: mechanisms of ammonium toxicity and the quest for tolerance. Plant Sci 248:92–101. CrossRefPubMedGoogle Scholar
  26. Granja F, Covarrubias JI (2018) Evaluation of acidifying nitrogen fertilizers in avocado trees with iron deficiency symptoms. J Soil Sci Plant Nutr 18:157–172. CrossRefGoogle Scholar
  27. Grusak MA (1995) Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): relevance to the iron nutrition of developing seeds. Planta 197:111–117. CrossRefGoogle Scholar
  28. Guo SH, Niu YJ, Zhai H, Han N, Du YP (2018) Effects of alkaline stress on organic acid metabolism in roots of grape hybrid rootstocks. Sci Hortic 227:255–260. CrossRefGoogle Scholar
  29. Hoopen FT, Cuin TA, Pedas P, Hegelund JN, Shabala S, Schjoerring JK, Jahn TP (2010) Competition between uptake of ammonium and potassium in barley and Arabidopsis roots: molecular mechanisms and physiological consequences. J Exp Bot 61:2303–2315. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Huang LL, Li MJ, Shao Y, Sun TT, Li CY, Ma FW (2018a) Ammonium uptake increases in response to PEG-induced drought stress in Malus hupehensis Rehd. Environ Exp Bot 151:32–42. CrossRefGoogle Scholar
  31. Huang LL, Li MJ, Zhou K, Sun TT, Hu LY, Li CY, Ma FW (2018b) Uptake and metabolism of ammonium and nitrate in response to drought stress in Malus prunifolia. Plant Physiol Biochem 127:185–193. CrossRefPubMedGoogle Scholar
  32. Jelali N, Dell’Orto M, Rabhi M, Zocchi G, Abdelly C, Gharsalli M (2010a) Physiological and biochemical responses for two cultivars of Pisum sativum (“Merveille de Kelvedon” and “Lincoln”) to iron deficiency conditions. Sci Hortic 124:116–121. CrossRefGoogle Scholar
  33. Jelali N, M’Sehli W, Dell’Orto M, Abdelly C, Gharsalli M, Zocchi G (2010b) Changes of metabolic responses to direct and induced Fe deficiency of two Pisum sativum cultivars. Environ Exp Bot 68:238–246. CrossRefGoogle Scholar
  34. Jiménez S, Gogorcena Y, Hévin C, Rombolà AD, Ollat N (2007) Nitrogen nutrition influences some biochemical responses to iron deficiency in tolerant and sensitive genotypes of Vitis. Plant Soil 290:343–355. CrossRefGoogle Scholar
  35. Kosegarten H, Koyro HW (2001) Apoplastic accumulation of iron in the epidermis of maize (Zea mays) roots grown in calcareous soil. Physiol Plant 113:515–522. CrossRefGoogle Scholar
  36. Ksouri R, Gharsalli M, Lachaâl M (2005) Physiological responses of Tunisian grapevine varieties to bicarbonate-induced iron deficiency. J Plant Physiol 162:335–341. CrossRefPubMedGoogle Scholar
  37. Ksouri R, M’Rah S, Gharsalli M, Lachaâl M (2006) Biochemical responses to true and bicarbonate-induced iron deficiency in grapevine genotypes. J Plant Nutr 29:305–315. CrossRefGoogle Scholar
  38. Ksouri R, Debez A, Mahmoudi H, Ouerghi Z, Gharsalli M, Lachaâl M (2007) Genotypic variability within Tunisian grapevine varieties (Vitis vinifera L.) facing bicarbonate-induced iron deficiency. Plant Physiol Biochem 45:315–322. CrossRefPubMedGoogle Scholar
  39. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. CrossRefGoogle Scholar
  40. Liu Y, von Wirén N (2017) Ammonium as a signal for physiological and morphological responses in plants. J Exp Bot 68:2581–2592. CrossRefPubMedGoogle Scholar
  41. Liu XF, Fan XF, Zhang LS, Yao CC, Long ZX, Wang XL (2002) Inducing factors of iron deficiency chlorosis of kiwis in Guanzhong area of Shaanxi. Acta Agric Boreali-occidentalis Sin 11:57–59Google Scholar
  42. López-Millán AF, Morales F, Abadía A, Abadía J (2000) Effects of iron deficiency on the composition of the leaf apoplastic fluid transport and xylem sap in sugar beet: implications for iron and carbon transport. Plant Physiol 124:873–884. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lucena JJ (2000) Effects of bicarbonate, nitrate and other environmental factors on iron deficiency chlorosis. a review. J Plant Nutr 23:1591–1606. CrossRefGoogle Scholar
  44. Lucena C, Romera FJ, Rojas CL, García MJ, Alcántara E, Pérez-Vicente R (2007) Bicarbonate blocks the expression of several genes involved in the physiological responses to Fe deficiency of Strategy I plants. Funct Plant Biol 34:1002–1009. CrossRefGoogle Scholar
  45. M’Sehli W, Youssfi S, Donnini S, Dell’Orto M, De Nisi P, Zocchi G, Abdelly C, Gharsalli M (2008) Root exudation and rhizosphere acidification by two lines of Medicago ciliaris in response to lime-induced iron deficiency. Plant Soil 312:151–162. CrossRefGoogle Scholar
  46. Ma BQ, Yuan YY, Gao M, Li CY, Ogutu C, Li MJ, Ma FW (2018) Determination of predominant organic acid components in Malus species: correlation with apple domestication. Metab 8:74. CrossRefGoogle Scholar
  47. Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, LondonGoogle Scholar
  48. Martínez-Cuenca M, Forner-Giner MA, Primo-Millo E, Legaz F (2013) The effect of sodium bicarbonate on plant performance and iron acquisition system of FA-5 (Forner-Alcaide 5) citrus seedlings. Acta Physiol Plant 35:2833–2845. CrossRefGoogle Scholar
  49. Mengel K (1994) Iron availability in plant tissues-iron chlorosis on calcareous soils. Plant Soil 165:275–283. CrossRefGoogle Scholar
  50. Michel L, Peña Á, Pastenes C, Berríos P, Rombolà AD, Covarrubias JI (2019) Sustainable strategies to prevent iron deficiency, improve yield and berry composition in blueberry (Vaccinium spp.). Front Plant Sci 10:255. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Molassiotis A, Tanou G, Diamantidis G, Patakas A, Therios I (2006) Effects of 4-month Fe deficiency exposure on Fe reduction mechanism, photosynthetic gas exchange, chlorophyll fluorescence and antioxidant defence in two peach rootstocks differing in Fe deficiency tolerance. J Plant Physiol 163:176–185. CrossRefPubMedGoogle Scholar
  52. Molina J, Covarrubias JI (2019) Influence of nitrogen on physiological responses to bicarbonate in a grapevine rootstock. J Soil Sci Plant Nutr. CrossRefGoogle Scholar
  53. Nikolic M, Romheld V, Merkt N (2000) Effect of bicarbonate on uptake and translocation of 59Fe in two grapevine rootstocks differing in their resistance to Fe deficiency chlorosis. Vitis 39:145–150Google Scholar
  54. O’Brien J, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutierrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856. CrossRefPubMedGoogle Scholar
  55. Ollat N, Laborde B, Neveux M, Diakou-Verdin P, Renaud C, Moing A (2003) Organic acid metabolism in roots of various grapevine (Vitis) rootstocks submitted to iron deficiency and bicarbonate nutrition. J Plant Nutr 26:2165–2176. CrossRefGoogle Scholar
  56. Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33:1486–1501. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rombolà AD, Brüggemann W, Tagliavini M, Marangoni B, Moog PR (2000) Iron source affects iron reduction and re-greening of kiwifruit (Actinidia deliciosa) leaves. J Plant Nutr 23:1751–1765. CrossRefGoogle Scholar
  58. Romera FJ, Alcántara E, de la Guardia MD (1997) Influence of bicarbonate and metal ions on the development of Fe(III) reducing capacity by Fe-deficient cucumber (Cucumis sativus) plants. Physiol Plant 101:143–148. CrossRefGoogle Scholar
  59. Rose MT, Rose TJ, Pariasca-Tanaka J, Widodo Wissuwa M (2011) Revisiting the role of organic acids in the bicarbonate tolerance of zinc-efficient rice genotypes. Funct Plant Biol 38:493–504. CrossRefGoogle Scholar
  60. Rose MT, Rose TJ, Pariasca-Tanaka J, Yoshihashi T, Neuweger H, Goesmann A, Frei M, Wissuwa M (2012) Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236:959–973. CrossRefPubMedGoogle Scholar
  61. Sahin O, Gunes A, Taskin MB, Inal A (2017) Investigation of responses of some apple (Mallus x domestica Borkh.) cultivars grafted on MM106 and M9 rootstocks to lime-induced chlorosis and oxidative stress. Sci Hortic 219:79–89. CrossRefGoogle Scholar
  62. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  63. Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Song XB, Zhang XW, Ma ST (2003) Studies on occurrence regulation of kiwifruit chlorosis. J Northwest Sci-Tech Univ Agric For (Nat Sci Ed) 31:5–8Google Scholar
  65. Susín S, Abadía A, González-Reyes JA, Lucena JJ, Abadía J (1996) The pH requirements for in vivo activity of the iron-deficiency “turbo” ferric chelate reductase. Plant Physiol 110:111–123. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tagliavini M, Rombolà AD (2001) Iron deficiency and chlorosis in orchard and vineyard ecosystems. Eur J Agron 15:71–92. CrossRefGoogle Scholar
  67. Tato L, De Nisi P, Donnini S, Zocchi G (2013) Low iron availability and phenolic metabolism in a wild plant species (Parietaria judaica L.). Plant Physiol Biochem 72:145–153. CrossRefPubMedGoogle Scholar
  68. Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70:1254–1257. CrossRefGoogle Scholar
  69. Tran LL, Ma HY, Tong YA, Lu YL, Lai Y, Liu F, Chen YJ, Lin W (2012) Nutrients diagnosis of kiwifruit chlorosis and study on relativity of soil nutrients. Soil Fert Sci 6:41–44Google Scholar
  70. Wang XQ, Li C, Liang D, Zou YJ, Li PM, Ma FW (2015) Phenolic compounds and antioxidant activity in red-fleshed apples. J Funct Foods 18:1086–1094. CrossRefGoogle Scholar
  71. Wang NN, Yao CC, Li MJ, Li CY, Liu ZD, Ma FW (2019) Anatomical and physiological responses of two kiwifruit cultivars to bicarbonate. Sci Hortic 243:528–536. CrossRefGoogle Scholar
  72. Yao CC, Long ZX, Liu XF (2005) Effect of iron deficiency chlorosis on kiwifruit. J Northwest For Univ 20:148–149Google Scholar
  73. Yu JY (2017) Efficient cultivation of kiwifruit in diagrams. China Machine Press, BeijingGoogle Scholar
  74. Yu JY, Liu ZD, Yao CC, Chen YA (2015) A new kiwifruit cultivar ‘Qihong’. Acta Hortic Sin 42:1409–1410Google Scholar
  75. Zhang KX, Wen T, Dong J, Bai TH, Wang K, Li CY (2016) Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. J Integr Agric 15:1499–1509. CrossRefGoogle Scholar
  76. Zou C, Fan X, Shi R, Zhang F (2007) Effect of ammonium and nitrate nitrogen on the growth and iron nutrition of up- and low-land rice. J China Agric Univ 12:45–49Google Scholar
  77. Zribi K, Gharsalli M (2002) Effect of bicarbonate on growth and iron nutrition of pea. J Plant Nutr 25:2143–2149. CrossRefGoogle Scholar
  78. Zuo Y, Ren L, Zhang F, Jiang RF (2007) Bicarbonate concentration as affected by soil water content controls iron nutrition of peanut plants in calcareous soil. Plant Physiol Biochem 45:357–364. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nannan Wang
    • 1
  • Xueyi Jiao
    • 1
  • Tianli Guo
    • 1
  • Cuiying Li
    • 1
  • Zhande Liu
    • 1
  • Fengwang Ma
    • 1
    Email author
  1. 1.State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of HorticultureNorthwest A and F UniversityYanglingChina

Personalised recommendations