Proline Metabolism and Its Functions in Development and Stress Tolerance

  • Maurizio TrovatoEmail author
  • Giuseppe Forlani
  • Santiago Signorelli
  • Dietmar FunckEmail author


Proline takes an exceptional place among the proteinogenic amino acids by its specific accumulation in pollen and in response to multiple types of stress. Despite more than 50 years of research, the biochemical pathways of proline biosynthesis and degradation still await their complete characterization in plants. Also, the molecular and physiological functions of proline metabolism in plant development and defense against stress are not yet fully understood. This chapter focuses on the current knowledge about the biochemical pathways of proline metabolism in plants, on its tissue-specific regulation and subcellular compartmentation, and on still open questions. Furthermore, we will summarize what is known about the influence of proline metabolism on plant development under optimal growth conditions and how it may support continued development despite the impact of stress. The cognate chapter “Regulation of Proline Accumulation and Its Molecular and Physiological Functions in Stress Defense” will focus on the possible beneficial functions of proline metabolism and accumulation in the defense response against diverse stresses. With these two cohesive chapters, we aim to provide a comprehensive picture of the current knowledge and the open research questions in proline-dependent stress defense.


Proline metabolism Gene expression Proline Plant development P5CS 


  1. Abrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372PubMedCrossRefGoogle Scholar
  2. Aleksza D, Horváth GV, Sándor G, Szabados L (2017) Proline accumulation is regulated by transcription factors associated with phosphate starvation. Plant Physiol 175:555–567. Scholar
  3. Armengaud P, Thiery L, Buhot N, Grenier-de March G, Savouré A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plant 120:442–450. Scholar
  4. Auclair JL, Jamieson CA (1948) A qualitative analysis of amino acids in pollen collected by bees. Science 108:357–358. Scholar
  5. Ayliffe MA, Mitchell HJ, Deuschle K, Pryor AJ (2005) Comparative analysis in cereals of a key proline catabolism gene. Mol Gen Genomics 274:494–505CrossRefGoogle Scholar
  6. Ayliffe MA, Roberts JK, Mitchell HJ, Zhang R, Lawrence GJ, Ellis JG, Pryor TJ (2002) A plant gene up-regulated at rust infection sites. Plant Physiol 129:169–180PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164. Scholar
  8. Bathurst NO (1954) The amino-acids of grass pollen. J Exp Bot 5:253–256. Scholar
  9. Besnard J, Pratelli R, Zhao C, Sonawala U, Collakova E, Pilot G, Okumoto S (2016) UMAMIT14 is an amino acid exporter involved in phloem unloading in Arabidopsis roots. J Exp Bot 67:6385–6397. Scholar
  10. Besnard J, Zhao C, Avice JC, Vitha S, Hyodo A, Pilot G, Okumoto S (2018) Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading. J Exp Bot 69:5221–5232. Scholar
  11. Bettini P, Michelotti S, Bindi D, Giannini R, Capuana M, Buaiatti M (2003) Pleiotropic effect of the insertion of Agrobacterium rhizogenes rolD gene in tomato (Lycopersicon esculentum Mill). Theor Appl Genet 107:831–836. Scholar
  12. Bhaskara GB, Yang T-H, Verslues PE (2015) Dynamic proline metabolism: importance and regulation in water limited environments. Front Plant Sci 6:484. Scholar
  13. Biancucci M, Mattioli R, Moubayidin L, Sabatini S, Costantino P, Trovato M (2015) Proline affects the size of the root meristematic zone in Arabidopsis. BMC Plant Biol 15:263. Scholar
  14. Boggess SF, Koeppe DE, Stewart CR (1978) Oxidation of proline by plant mitochondria. Plant Physiol 62:22–25PubMedPubMedCentralCrossRefGoogle Scholar
  15. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291. Scholar
  16. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, RockvilleGoogle Scholar
  17. Büssis D, Heineke D (1998) Acclimation of potato plants to polyethylene glycol-induced water deficit II. Contents and subcellular distribution of organic solutes. J Exp Bot 49:1361–1370CrossRefGoogle Scholar
  18. Cabassa-Hourton C et al (2016) Proteomic and functional analysis of proline dehydrogenase 1 link proline catabolism to mitochondrial electron transport in Arabidopsis thaliana. Biochem J 473:2623–2634. Scholar
  19. Canas RA, Villalobos DP, Diaz-Moreno SM, Canovas FM, Canton FR (2008) Molecular and functional analyses support a role of Ornithine-{delta}-aminotransferase in the provision of glutamate for glutamine biosynthesis during pine germination. Plant Physiol 148:77–88PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cecchini NM, Monteoliva MI, Alvarez ME (2011) Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiol 155:1947–1959. Scholar
  21. Chen Q, Zheng Y, Luo L, Yang Y, Hu X, Kong X (2018) Functional FRIGIDA allele enhances drought tolerance by regulating the P5CS1 pathway in Arabidopsis thaliana. Biochem Biophys Res Commun 495:1102–1107. Scholar
  22. Chiang HH, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis thaliana (L) Heynh during development and in response to desiccation. Plant Cell Environ 18:1280–1290. Scholar
  23. Chinnusamy V, Zhu J-K (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139. Scholar
  24. da Rocha IM, Vitorello VA, Silva JS, Ferreira-Silva SL, Viégas RA, Silva EN, Silveira JA (2012) Exogenous ornithine is an effective precursor and the delta-ornithine amino transferase pathway contributes to proline accumulation under high N recycling in salt-stressed cashew leaves. J Plant Physiol 169:41–49. Scholar
  25. Daygon VD et al (2017) Metabolomics and genomics combine to unravel the pathway for the presence of fragrance in rice. Sci Rep 7:8767. Scholar
  26. De Ronde JA, Cress WA, Kruger GH, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224PubMedCrossRefGoogle Scholar
  27. Delauney AJ, Hu CA, Kishor PB, Verma DP (1993) Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268:18673–18678PubMedGoogle Scholar
  28. Delauney AJ, Verma DP (1990) A soybean gene encoding delta 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet 221:299–305CrossRefGoogle Scholar
  29. Deuschle K et al (2004) The role of δ1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425PubMedPubMedCentralCrossRefGoogle Scholar
  30. Deuschle K, Funck D, Hellmann H, Däschner K, Binder S, Frommer WB (2001) A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J 27:345–356. Scholar
  31. Di Martino C, Pizzuto R, Pallotta ML, De Santis A, Passarella S (2006) Mitochondrial transport in proline catabolism in plants: the existence of two separate translocators in mitochondria isolated from durum wheat seedlings. Planta 223:1123–1133PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dietrich K, Weltmeier F, Ehlert A, Weiste C, Stahl M, Harter K, Dröge-Laser W (2011) Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell 23:381–395. Scholar
  33. Dinkeloo K, Boyd S, Pilot G (2018) Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Semin Cell Dev Biol 74:105–113. Scholar
  34. Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67:780–784PubMedPubMedCentralCrossRefGoogle Scholar
  35. Elthon TE, Stewart CR (1982) Proline oxidation in corn mitochondria : involvement of NAD, relationship to ornithine metabolism, and sidedness on the inner membrane. Plant Physiol 70:567–572PubMedPubMedCentralCrossRefGoogle Scholar
  36. Elthon TE, Stewart CR, Bonner WD (1984) Energetics of proline transport in corn mitochondria. Plant Physiol 75:951–955PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant-Microbe Interact 17:343–350PubMedCrossRefGoogle Scholar
  38. Faes P et al (2015) Molecular evolution and transcriptional regulation of the oilseed rape proline dehydrogenase genes suggest distinct roles of proline catabolism during development. Planta 241:403–419. Scholar
  39. Falasca G, Altamura MM, D’Angeli S, Zaghi D, Costantino P, Mauro ML (2010) The rolD oncogene promotes axillary bud and adventitious root meristems in Arabidopsis. Plant Physiol Biochem 48:797–804. Scholar
  40. Feng XJ, Li JR, Qi SL, Lin QF, Jin JB, Hua XJ (2016) Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc Natl Acad Sci U S A 113:E8335–e8343. Scholar
  41. Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka L (2015) Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev Camb Philos Soc 90:1065–1099. Scholar
  42. Fischer WN, Kwart M, Hummel S, Frommer WB (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J Biol Chem 270:16315–16320CrossRefGoogle Scholar
  43. Forlani G, Bertazzini M, Zarattini M, Funck D, Ruszkowski M, Nocek B (2015) Functional properties and structural characterization of rice delta(1)-pyrroline-5-carboxylate reductase. Front Plant Sci 6:565. Scholar
  44. Forlani G, Scainelli D, Nielsen E (1997) δ1-Pyrroline-5-carboxylate dehydrogenase from cultured cells of potato (purification and properties). Plant Physiol 113:1413–1418PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fujiki Y, Teshima H, Kashiwao S, Kawano-Kawada M, Ohsumi Y, Kakinuma Y, Sekito T (2017) Functional identification of AtAVT3, a family of vacuolar amino acid transporters, in Arabidopsis. FEBS Lett 591:5–15. Scholar
  46. Fujita T, Maggio A, Garcia-Rios M, Bressan RA, Csonka LN (1998) Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Delta1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiol 118:661–674PubMedPubMedCentralCrossRefGoogle Scholar
  47. Funck D, Eckard S, Müller G (2010) Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. BMC Plant Biol 10:70. Scholar
  48. Funck D, Mattioli R, Biancucci M, Mosca L, Trovato M (2019) Proline biosynthesis: localisation matters. Paper presented at the 32nd Conference Molecular Biology of Plants, Dabringhausen, Germany,Google Scholar
  49. Funck D, Stadelhofer B, Koch W (2008) Ornithine-δ-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biol 8:40. Scholar
  50. Funck D, Winter G, Baumgarten L, Forlani G (2012) Requirement of proline synthesis during Arabidopsis reproductive development. BMC Plant Biol 12:191. Scholar
  51. Giberti S, Funck D, Forlani G (2014) Δ1-Pyrroline-5-carboxylate reductase from Arabidopsis thaliana: stimulation or inhibition by chloride ions and feedback regulation by proline depend on whether NADPH or NADH acts as co-substrate. New Phytol 202:911–919. Scholar
  52. Ginguay A, Cynober L, Curis E, Nicolis I (2017) Ornithine aminotransferase, an important glutamate-metabolizing enzyme at the crossroads of multiple metabolic pathways. Biology 6. Scholar
  53. Girousse C, Bournoville R, Bonnemain J-L (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111:109–113PubMedPubMedCentralCrossRefGoogle Scholar
  54. Goodman JL, Wang S, Alam S, Ruzicka FJ, Frey PA, Wedekind JE (2004) Ornithine cyclodeaminase: structure, mechanism of action, and implications for the mu-crystallin family. Biochemistry 43:13883–13891. Scholar
  55. Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus JM, Rentsch D (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137:117–126PubMedPubMedCentralCrossRefGoogle Scholar
  56. Guan C, Huang YH, Cui X, Liu SJ, Zhou YZ, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline-biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199. Scholar
  57. Hanson J, Hanssen M, Wiese A, Hendriks MMWB, Smeekens S (2008) The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2. Plant J 53:935–949. Scholar
  58. Hare P, Cress W, van Staden J (2003) A regulatory role for proline metabolism in stimulating Arabidopsis thaliana seed germination. Plant Growth Regul 39:41–50CrossRefGoogle Scholar
  59. Hayashi F, Ichino T, Osanai M, Wada K (2000) Oscillation and regulation of proline content by P5CS and ProDH gene expressions in the light/dark cycles in Arabidopsis thaliana L. Plant Cell Physiol 41:1096–1101. Scholar
  60. Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 123:779–789PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hildebrandt TM (2018) Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol Biol 98:121–135. Scholar
  62. Hill RW, Wyse GA, Anderson M (2016) Animal physiology. Sinauer Associates, SunderlandGoogle Scholar
  63. Hirner A et al (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946. Scholar
  64. Hong-qi Z, Croes AF, Linskens HF (1982) Protein synthesis in germinating pollen of Petunia: role of proline. Planta 154:199–203. Scholar
  65. Hu CA, Delauney AJ, Verma DP (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci U S A 89:9354–9358PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hua XJ, van de Cotte B, Van Montagu M, Verbruggen N (1997) Developmental regulation of pyrroline-5-carboxylate reductase gene expression in Arabidopsis. Plant Physiol 114:1215–1224PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hua XJ, van de Cotte B, Van Montagu M, Verbruggen N (2001) The 5′ untranslated region of the At-P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J 26:157–169PubMedCrossRefGoogle Scholar
  68. Hua-long L, Han-jing S, Jing-guo W, Yang L, De-tang Z, Hong-wei Z (2014) Effect of seed soaking with exogenous proline on seed germination of rice under salt stress. J Northeast Aric Univ 21:1–6. Scholar
  69. Huang AHC, Cavalieri AJ (1979) Proline oxidase and water stress-induced proline accumulation in spinach leaves. Plant Physiol 63:531–535PubMedPubMedCentralCrossRefGoogle Scholar
  70. Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS One 7:e40203. Scholar
  71. Kavi Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394. Scholar
  72. Kavi Kishor PB, Hima Kumari P, Sunita MSL, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544. Scholar
  73. Kesari R et al (2012) Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation. Proc Natl Acad Sci U S A 109:9197–9202. Scholar
  74. Khan MR, Ai XY, Zhang JZ (2014) Genetic regulation of flowering time in annual and perennial plants. Wiley Interdiscip Rev RNA 5:347–359. Scholar
  75. Kim G-B, Nam Y-W (2013) A novel Δ1-pyrroline-5-carboxylate synthetase gene of Medicago truncatula plays a predominant role in stress-induced proline accumulation during symbiotic nitrogen fixation. J Plant Physiol 170:291–302. Scholar
  76. Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335. Scholar
  77. Korasick DA et al (2019) Structural and biochemical characterization of Aldehyde Dehydrogenase 12, the last enzyme of proline catabolism in plants. J Mol Biol 431:576–592. Scholar
  78. Kubala S, Wojtyla Ł, Quinet M, Lechowska K, Lutts S, Garnczarska M (2015) Enhanced expression of the proline synthesis gene P5CSA in relation to seed osmopriming improvement of Brassica napus germination under salinity stress. J Plant Physiol 183:1–12. Scholar
  79. Ladwig F et al (2012) Siliques Are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol 158:1643–1655. Scholar
  80. Lehmann S, Gumy C, Blatter E, Boeffel S, Fricke W, Rentsch D (2011) In planta function of compatible solute transporters of the AtProT family. J Exp Bot 62:787–796. Scholar
  81. Lichtenthaler HK (1998) The stress concept in plants: an introduction. Ann N Y Acad Sci 851:187–198. Scholar
  82. Liu C et al (2018) Ornithine δ-aminotransferase is critical for floret development and seed setting through mediating nitrogen reutilization in rice. Plant J 96:842–854. Scholar
  83. Ma L, Zhou E, Gao L, Mao X, Zhou R, Jia J (2008) Isolation, expression analysis and chromosomal location of P5CR gene in common wheat (Triticum aestivum L.). S Afr J Bot 74:705CrossRefGoogle Scholar
  84. Mani S, Van De Cotte B, Van Montagu M, Verbruggen N (2002) Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiol 128:73–83PubMedPubMedCentralCrossRefGoogle Scholar
  85. Mattioli R, Biancucci M, El Shall A, Mosca L, Costantino P, Funck D, Trovato M (2018) Proline synthesis in developing microspores is required for pollen development and fertility. BMC Plant Biol 18:356. Scholar
  86. Mattioli R, Biancucci M, Lonoce C, Costantino P, Trovato M (2012) Proline is required for male gametophyte development in Arabidopsis. BMC Plant Biol 12:236. Scholar
  87. Mattioli R, Falasca G, Sabatini S, Altamura MM, Costantino P, Trovato M (2009) The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiol Plant 137:72–85. Scholar
  88. Mattioli R, Marchese D, D'Angeli S, Altamura MM, Costantino P, Trovato M (2008) Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol Biol 66:277–288. Scholar
  89. Mauro ML, Trovato M, De Paolis A, Gallelli A, Costantino P, Altamura MM (1996) The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Dev Biol 180:693–700. Scholar
  90. Meister A, Radhakrishnan AN, Buckley SD (1957) Enzymatic synthesis of L-pipecolic acid and L-proline. J Biol Chem 229:789–800PubMedGoogle Scholar
  91. Mestichelli LJ, Gupta RN, Spenser ID (1979) The biosynthetic route from ornithine to proline. J Biol Chem 254:640–647PubMedGoogle Scholar
  92. Mezl VA, Knox WE (1976) Properties and analysis of a stable derivative of pyrroline-5-carboxylic acid for use in metabolic studies. Anal Biochem 74:430–440PubMedCrossRefGoogle Scholar
  93. Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009) Unraveling δ1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J Biol Chem 284:26482–26492. Epub 22009 Jul 26427PubMedPubMedCentralCrossRefGoogle Scholar
  94. Mitchell HJ, Ayliffe MA, Rashid KY, Pryor AJ (2006) A rust-inducible gene from flax (fis1) is involved in proline catabolism. Planta 223:213–222CrossRefGoogle Scholar
  95. Monne M et al (2018) Uncoupling proteins 1 and 2 (UCP1 and UCP2) from Arabidopsis thaliana are mitochondrial transporters of aspartate, glutamate, and dicarboxylates. J Biol Chem 293:4213–4227. Scholar
  96. Monteoliva MI, Rizzi YS, Cecchini NM, Hajirezaei MR, Alvarez ME (2014) Context of action of proline dehydrogenase (ProDH) in the hypersensitive response of Arabidopsis. BMC Plant Biol 14:21. Scholar
  97. Moxley MA, Zhang L, Christgen S, Tanner JJ, Becker DF (2017) Identification of a conserved histidine as being critical for the catalytic mechanism and functional switching of the multifunctional Proline utilization A protein. Biochemistry 56:3078–3088. Scholar
  98. Müller B et al (2015) Amino acid export in developing Arabidopsis seeds depends on UmamiT facilitators. Curr Biol 25:3126–3131. Scholar
  99. Murahama M, Yoshida T, Hayashi F, Ichino T, Sanada Y, Wada K (2001) Purification and characterization of Delta(1)-pyrroline-5-carboxylate reductase isoenzymes, indicating differential distribution in spinach (Spinacia oleracea L.) leaves. Plant Cell Physiol 42:742–750PubMedPubMedCentralCrossRefGoogle Scholar
  100. Mutters RG, Ferreira LGR, Hall AE (1989) Proline content of the anthers and pollen of heat-tolerant and heat-sensitive cowpea subjected to different temperatures. Crop Sci 29:1497–1500CrossRefGoogle Scholar
  101. Nakashima K, Satoh R, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1998) A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. Plant Physiol 118:1233–1241. Scholar
  102. Nanjo T, Fujita M, Seki M, Kato T, Tabata S, Shinozaki K (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell Physiol 44:541–548PubMedCrossRefGoogle Scholar
  103. Nanjo T et al (1999a) Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J 18:185–193PubMedCrossRefGoogle Scholar
  104. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999b) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210. Scholar
  105. Noguchi M, Koiwai A, Tamaki E (1966) Studies on nitrogen metabolism in tobacco plants. Agric Biol Chem 30:452–456. Scholar
  106. Nozaki H (2005) A new scenario of plastid evolution: plastid primary endosymbiosis before the divergence of the “Plantae,” emended. J Plant Res 118:247–255. Scholar
  107. O'Hara LE, Paul MJ, Wingler A (2013) How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol Plant 6:261–274. Scholar
  108. Peng Z, Lu Q, Verma DPS (1996) Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Gen Genet 253:334–341. Scholar
  109. Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140. Scholar
  110. Perchlik M, Foster J, Tegeder M (2014) Different and overlapping functions of Arabidopsis LHT6 and AAP1 transporters in root amino acid uptake. J Exp Bot 65:5193–5204. Scholar
  111. Pohlmeyer K, Soll J, Steinkamp T, Hinnah S, Wagner R (1997) Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proc Natl Acad Sci U S A 94:9504–9509. Scholar
  112. Porcelli V et al (2018) Molecular identification and functional characterization of a novel glutamate transporter in yeast and plant mitochondria. Biochim Biophys Acta 1859:1249–1258. Scholar
  113. Posmyk MM, Janas KM (2007) Effects of seed hydropriming in presence of exogenous proline on chilling injury limitation in Vigna radiata L. seedlings. Acta Physiol Plant 29:509–517. Scholar
  114. Rayapati PJ, Stewart CR, Hack E (1989) Pyrroline-5-carboxylate reductase is in pea (Pisum sativum L.) leaf chloroplasts. Plant Physiol 91:581–586PubMedPubMedCentralCrossRefGoogle Scholar
  115. Ren Y et al (2018) DFR1-mediated inhibition of proline degradation pathway regulates drought and freezing tolerance in Arabidopsis. Cell Rep 23:3960–3974. Scholar
  116. Rena AB, Splittstoesser WE (1975) Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons. Phytochemistry 14:657–661. Scholar
  117. Renné P, Dreßen U, Hebbeker U, Hille D, Flügge U-I, Westhoff P, Weber APM (2003) The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J 35:316–331. Scholar
  118. Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446PubMedPubMedCentralGoogle Scholar
  119. Richards EJ (2006) Inherited epigenetic variation - revisiting soft inheritance. Nat Rev Genet 7:395. Scholar
  120. Roosens NH, Al Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine-delta-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80CrossRefGoogle Scholar
  121. Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271. Scholar
  122. Ruszkowski M, Nocek B, Forlani G, Dauter Z (2015) The structure of Medicago truncatula delta(1)-pyrroline-5-carboxylate reductase provides new insights into regulation of proline biosynthesis in plants. Front Plant Sci 6:869. Scholar
  123. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer ZS, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616. Scholar
  124. Sangwan RS (1978) Change in the amino-acid content during male gametophyte formation of Datura metel in situ. Theor Appl Genet 52:221–225. Scholar
  125. Satoh R, Nakashima K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2002) ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis. Plant Physiol 130:709–719. Scholar
  126. Savouré A, Jaoua S, Hua X-J, Ardiles W, Van Montagu M, Verbruggen N (1995) Isolation, characterization, and chromosomal location of a gene encoding the Δ1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett 372:13–19. Scholar
  127. Savouré A, Jaoua S, Hua XJ, Ardiles W, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet 254:104–109. Scholar
  128. Schertl P, Cabassa C, Saadallah K, Bordenave M, Savouré A, Braun HP (2014) Biochemical characterization of proline dehydrogenase in Arabidopsis mitochondria. FEBS J 281:2794–2804. Scholar
  129. Schmidt R, Stransky H, Koch W (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226:805–813. Scholar
  130. Schulze WX, Yao Q, Xu D (2015) Databases for plant phosphoproteomics. Methods Mol Biol 1306:207–216. Scholar
  131. Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11:377–392. Scholar
  132. Sharma S, Shinde S, Verslues PE (2013) Functional characterization of an ornithine cyclodeaminase-like protein of Arabidopsis thaliana. BMC Plant Biol 13:182. Scholar
  133. Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157:292–304. Scholar
  134. Shetty K, Wahlqvist ML (2004) A model for the role of the proline-linked pentose-phosphate pathway in phenolic phytochemical bio-synthesis and mechanism of action for human health and environmental applications. Asia Pac J Clin Nutr 13:1–24PubMedGoogle Scholar
  135. Shinde S, Villamor JG, Lin W, Sharma S, Verslues PE (2016) Proline coordination with fatty acid synthesis and redox metabolism of chloroplast and mitochondria. Plant Physiol 172:1074–1088. Scholar
  136. Shui XR, Chen ZW, Li JX (2013) MicroRNA prediction and its function in regulating drought-related genes in cowpea. Plant Sci 210:25–35. Scholar
  137. Signorelli S, Monza J (2017) Identification of Δ1-pyrroline 5-carboxylate synthase (P5CS) genes involved in the synthesis of proline in Lotus japonicus. Plant Signal Behav 12:e1367464. Scholar
  138. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037. Scholar
  139. Stines AP, Naylor DJ, Høj PB, van Heeswijck R (1999) Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of Δ1-Pyrroline-5-Carboxylate Synthetase mRNA or protein. Plant Physiol 120:923–923. Scholar
  140. Stránská J, Kopecný D, Tylichová M, Snégaroff J, Sebela M (2008) Ornithine delta-aminotransferase: an enzyme implicated in salt tolerance in higher plants. Plant Signal Behav 3:929–935PubMedPubMedCentralCrossRefGoogle Scholar
  141. Strecker HJ (1965) Purification and properties of rat liver ornithine δ-transaminase. J Biol Chem 240:1225–1230PubMedGoogle Scholar
  142. Strizhov N et al (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12:557–569. Scholar
  143. Székely G et al (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28. Scholar
  144. Szoke A, Miao GH, Hong Z, Verma DP (1992) Subcellular location of δ1-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean. Plant Physiol 99:1642–1649PubMedPubMedCentralCrossRefGoogle Scholar
  145. Taiz L, Zeiger E, Møller IM, Murphy A (2018) Fundamentals of plant physiology. Oxford University Press, New York/OxfordGoogle Scholar
  146. Tanner JJ (2019) Structural biology of proline catabolic enzymes. Antioxid Redox Signal 30:650–673. Scholar
  147. Taylor AA, Stewart GR (1981) Tissue and subcellular localization of enzymes of arginine metabolism in Pisum sativum. Biochem Biophys Res Commun 101:1281–1289PubMedCrossRefGoogle Scholar
  148. Tegeder M, Hammes UZ (2018) The way out and in: phloem loading and unloading of amino acids. Curr Opin Plant Biol 43:16–21. Scholar
  149. Thiery L, Leprince AS, Lefebvre D, Ghars MA, Debarbieux E, Savouré A (2004) Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis thaliana. J Biol Chem 279:14812–14818. Scholar
  150. Trovato M, Maras B, Linhares F, Costantino P (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proc Natl Acad Sci U S A 98:13449.13453. Scholar
  151. Trovato M, Mattioli R, Costantino P (2018) From A. rhizogenes RolD to plant P5CS: exploiting proline to control plant development. Plan Theory 7:108Google Scholar
  152. Trovato M, Mauro ML, Costantino P, Altamura MM (1997) The rolD gene from Agrobacterium rhizogenes is developmentally regulated in transgenic tobacco. Protoplasma 197:111–120. Scholar
  153. Turchetto-Zolet AC, Margis-Pinheiro M, Margis R (2009) The evolution of pyrroline-5-carboxylate synthase in plants: a key enzyme in proline synthesis. Mol Gen Genomics 281:87–97CrossRefGoogle Scholar
  154. Van Aken O, Zhang B, Carrie C, Uggalla V, Paynter E, Giraud E, Whelan J (2009) Defining the mitochondrial stress response in Arabidopsis thaliana. Mol Plant 2:1310–1324. Scholar
  155. Vansuyt G, Vallee J-C, Prevost J (1979) La pyrroline-5-carboxylate réductase et la proline déhydrogénase chez Nicotiana tabacum var. Xanthi n.c. en fonction de son développement. Physiologie végétale 19:95–105Google Scholar
  156. Veerabagu M et al (2014) The interaction of the Arabidopsis response regulator ARR18 with bZIP63 mediates the regulation of PROLINE DEHYDROGENASE expression. Mol Plant 7:1560–1577. Scholar
  157. Venekamp JH, Koot JTM (1988) The sources of free proline and asparagine in field bean plants, Vicia faba L., during and after a short period of water withholding. J Plant Physiol 32:102–109CrossRefGoogle Scholar
  158. Verbruggen N, Hua XJ, May M, Van Montagu M (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc Natl Acad Sci U S A 93:8787–8791. Scholar
  159. Verbruggen N, Villarroroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103:771–781PubMedPubMedCentralCrossRefGoogle Scholar
  160. Verslues PE, Skarp RE (1999) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiol 119:1349–1360PubMedPubMedCentralCrossRefGoogle Scholar
  161. Wada KC, Takeno K (2010) Stress-induced flowering. Plant Signal Behav 5:944–947. Scholar
  162. Wakte K, Zanan R, Hinge V, Khandagale K, Nadaf A, Henry R (2017) Thirty-three years of 2-acetyl-1-pyrroline, a principal basmati aroma compound in scented rice (Oryza sativa L.): a status review. J Sci Food Agric 97:384–395. Scholar
  163. Walton EF, Clark CJ, Boldingh HL (1991) Effect of hydrogen cyanamide on amino acid profiles in kiwifruit buds during bud-break. Plant Physiol 97:1256–1259PubMedPubMedCentralCrossRefGoogle Scholar
  164. Wanduragala S, Sanyal N, Liang X, Becker DF (2010) Purification and characterization of Put1p from Saccharomyces cerevisiae. Arch Biochem Biophys 498:136–142. Scholar
  165. Wang G et al (2014) Proline responding1 plays a critical role in regulating general protein synthesis and the cell cycle in Maize. Plant Cell 26:2582–2600. Scholar
  166. Wang T, Chen Y, Zhang M, Chen J, Liu J, Han H, Hua X (2017) Arabidopsis AMINO ACID PERMEASE1 contributes to salt stress-induced proline uptake from exogenous sources. Front Plant Sci 8:2182. Scholar
  167. Watanabe S, Tanimoto Y, Yamauchi S, Tozawa Y, Sawayama S, Watanabe Y (2014) Identification and characterization of trans-3-hydroxy-l-proline dehydratase and Delta(1)-pyrroline-2-carboxylate reductase involved in trans-3-hydroxy-l-proline metabolism of bacteria. FEBS Open Bio 4:240–250. Scholar
  168. Weiste C et al (2017) The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth. PLoS Genet 13:e1006607. Scholar
  169. Weltmeier F et al (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143. Scholar
  170. White FF, Taylor BH, Huffman GA, Nester EW (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164:33–44PubMedPubMedCentralGoogle Scholar
  171. Yang J, Zhang N, Ma C, Qu Y, Si H, Wang D (2013) Prediction and verification of microRNAs related to proline accumulation under drought stress in potato. Comput Biol Chem 46:48–54. Scholar
  172. Yoshiba Y, Nanjo T, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem Biophys Res Commun 261:766–772PubMedCrossRefGoogle Scholar
  173. Yoshihashi T, Huong NT, Inatomi H (2002) Precursors of 2-acetyl-1-pyrroline, a potent flavor compound of an aromatic rice variety. J Agric Food Chem 50:2001–2004PubMedCrossRefGoogle Scholar
  174. You J, Hu H, Xiong L (2012) An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci 197:59–69. Scholar
  175. Zarattini M, Forlani G (2017) Toward unveiling the mechanisms for transcriptional regulation of proline biosynthesis in the plant cell response to biotic and abiotic stress conditions. Front Plant Sci 8.
  176. Zhang CS, Lu Q, Verma DP (1995) Removal of feedback inhibition of delta 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. J Biol Chem 270:20491–20496CrossRefGoogle Scholar
  177. Zhang CY, Wang NN, Zhang YH, Feng QZ, Yang CW, Liu B (2013) DNA methylation involved in proline accumulation in response to osmotic stress in rice (Oryza sativa). Genet Mol Res 12:1269–1277. Scholar
  178. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48. Scholar
  179. Zonglie H, Karuna L, Zhongming Z, Verma DPS (2000) Removal of feedback inhibition of Δ1-Pyrroline-5-Carboxylate Synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136. Scholar

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Authors and Affiliations

  1. 1.Department of Biology and BiotechnologySapienza University of RomeRomeItaly
  2. 2.Department of Life Science and BiotechnologyUniversity of FerraraFerraraItaly
  3. 3.Department of Plant BiologyUniversidad de la RepúblicaMontevideoUruguay
  4. 4.Department of Biology, Division of Plant Physiology and BiochemistryUniversity of KonstanzKonstanzGermany

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