Advertisement

Drought-induced proline synthesis depends on root-to-shoot communication mediated by light perception

  • D. C. Ferreira Júnior
  • L. A. Gaion
  • G. S. Sousa Júnior
  • D. M. M. Santos
  • R. F. CarvalhoEmail author
Short Communication

Abstract

Proline accumulation in roots and shoots is one of the most evident responses to environmental stresses such as drought, which is currently one of the main threats for agriculture. Based on this response, in this work, we hypothesize that proline accumulation is dependent on root-to-shoot communication through light perception. Thus, we used exaggerated light response (hp1) and phytochrome-deficient (au) mutants of tomato, which were combined through self-grafting and reciprocal grafting and subjected to drought stress, for posterior determination of shoot and root growth and proline content. Light-affected proline metabolism, as hp1, had the highest accumulation, while au presented the lowest proline values. Reciprocal grafting showed that hp1 and MT as scion or rootstock improved MT and au proline content, respectively, indicating shoot-to-root and root-to-shoot communication modulate the metabolism of this compatible osmolyte. Dry weight, leaf area, and root area presented similar patterns to proline content, indicating the importance of this compound for plant growth under stress conditions. These results provide a new perspective on light mediation of long-distance proline translocation in stressed plants.

Keywords

Phytochromes Compatible osmolyte Drought stress Light signaling 

References

  1. Ábrahám E, Rigó G, Szekély 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 51:363–372.  https://doi.org/10.1023/A:1022043000516 CrossRefPubMedGoogle Scholar
  2. Alves FRR, Melo HC, Crispim-Filho AJ, Costa AC, Nascimento RJT, Carvalho RF (2016) Physiological and biochemical responses of photomorphogenic tomato mutants (cv. Micro-Tom) under water withholding. Acta Physiol Plant 38:155–158.  https://doi.org/10.1007/s11738-016-2169-8 CrossRefGoogle Scholar
  3. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207.  https://doi.org/10.1007/BF00018060 CrossRefGoogle Scholar
  4. Bojórquez-Quintal E, Valrde-Buendía A, Ku-González A, Carillo-Pech M, Ortega-Camacho D, Echevarría-Machado I, Pottosin I, Martínez-Estévez M (2014) Mechanisms of salt tolerance in habanero pepper plants (Capsicum chinense Jacq.): proline accumulation, ions dynamics and sodium root-shoot partition and compartmentation. Front Plant Sci 5:605.  https://doi.org/10.3389/fpls.2014.00605 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bundig C, Vu TH, Meise P, Seddig S, Schum A, Winkelmann T (2016) Variability in osmotic stress tolerance of starch potato genotypes (Solanum tuberosum L.) as revealed by an in vitro screening: role of proline, osmotic adjustment and drought response in pot trials. J Agron Crop Sci 203:206–218.  https://doi.org/10.1111/jac.12186 CrossRefGoogle Scholar
  6. Chen LY, Shi DQ, Zhang WJ, Tang ZS, Liu J, Yang WC (2015) The Arabidopsis alkaline ceramidase TOD1 is a key turgor pressure regulator in plant cells. Nat Commun 6:6030.  https://doi.org/10.1038/ncomms7030 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442.  https://doi.org/10.3389/fpls.2013.00442 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dong C, Fu Y, Liu G, Liu H (2014) Low light intensity effects on the growth, photosynthetic characteristics, antioxidant capacity, yield and quality of wheat (Triticum aestivum L.) at different growth stages in BLSS. Adv Space Res 53:1557–1566.  https://doi.org/10.1016/j.asr.2014.02.004 CrossRefGoogle Scholar
  9. 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 USA 113:8335–8343.  https://doi.org/10.1073/pnas.1610670114 CrossRefGoogle Scholar
  10. Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN (2015) Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev Camb Philos Soc 90:1065–1099.  https://doi.org/10.1111/brv.12146 CrossRefPubMedGoogle Scholar
  11. Fillipou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot J 97:1–10.  https://doi.org/10.1016/j.envexpbot.2013.09.010 CrossRefGoogle Scholar
  12. Girousse C, Bournoville R, Bonnemain JL (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111:109–113.  https://doi.org/10.1104/pp.111.1.109 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kendrick RE, Kerckhoffs LHJ, Van Tuinen A, Koornneef M (1997) Photomorphogenic mutants of tomato. Plant Cell Environ 20:746–751.  https://doi.org/10.1046/j.1365-3040.1997.d01-109.x CrossRefGoogle Scholar
  14. Liu YS, Roof S, Ye ZB, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902.  https://doi.org/10.1073/pnas.0400935101 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Monteiro CC, Rolão MB, Franco MR, Peters LP, Cia MC, Capaldi FR, Carvalho RF, Gratão PL, Rossi ML, Martinelli AP, Peres LEP, Azevedo RA (2012) Biochemical and histological characterization of tomato mutants. An Acad Bras Cienc 84:573–585.  https://doi.org/10.1590/S0001-37652012005000022 CrossRefPubMedGoogle Scholar
  16. Muramoto T, Kami C, Kataoka H, Iwata N, Linley PJ, Mukougawa K, Yokota A, Kohchi T (2005) The tomato photomorphogenetic mutant, aurea, is deficient in phytochromobilin synthase for phytochrome chromophore biosynthesis. Plant Cell Physiol 46:661–665.  https://doi.org/10.1093/pcp/pci062 CrossRefPubMedGoogle Scholar
  17. Rejeb KB, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284.  https://doi.org/10.1016/j.plaphy.2014.04.007 CrossRefPubMedGoogle Scholar
  18. Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiol 164:1772–1788.  https://doi.org/10.1104/pp.113.221424 CrossRefPubMedGoogle Scholar
  19. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726.  https://doi.org/10.1093/jxb/erj073 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  1. 1.School of Agricultural and Veterinarian SciencesSão Paulo State University (Unesp)JaboticabalBrazil

Personalised recommendations