Photosynthetica 2018, 56(1):404-410 | DOI: 10.1007/s11099-018-0784-x

Loss of photosynthesis signals a metabolic reprogramming to sustain sugar homeostasis during senescence of green leaves: Role of cell wall hydrolases

B. Biswal1,*, J. K. Pandey1
1 Laboratory of Biochemistry and Molecular Biology, School of Life Sciences, Sambalpur University, Jyoti Vihar, Burla, Odisha, India

Leaf senescence is always associated with decline in photosynthesis, consequently a loss of cellular sugar. On the other hand, execution of senescence program needs energy and leaves, therefore, tend to collect sugars from other sources to sustain energy homeostasis. This sugar reprogramming induced by loss of sugar involves operation of a complex catabolic network. The exact molecular mechanism of induction and regulation of the network, however, is not fully resolved but the current literature available suggests sugar starvation as a signal for induction of several senescence-associated genes including the genes coding for the enzymes for degradation of cellular constituents and their conversion to respiratory sugars. The late expression of genes coding for the cell wall hydrolases and enhancement in the activity of these enzymes late during senescence are indicative of the cell wall polysaccharides as the last source of sugars to sustain energy homeostasis for execution of the senescence program.

Additional key words: cell wall hydrolases; photosynthesis; senescence; sugar homeostasis

Received: August 4, 2017; Accepted: September 27, 2017; Published: March 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Biswal, B., & Pandey, J.K. (2018). Loss of photosynthesis signals a metabolic reprogramming to sustain sugar homeostasis during senescence of green leaves: Role of cell wall hydrolases. Photosynthetica, 56(SPECIAL ISSUE), 404-410. doi: 10.1007/s11099-018-0784-x
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aguilera-Alvarado G.P., Sánchez-Nieto S.: Plant hexokinases are multifaceted proteins.-Plant Cell Physiol. 58: 1151-1160, 2017. Go to original source...
    2. Avila-Ospina L., Moison M., Yoshimoto K., Masclaux-Daubresse C.: Autophagy, plant senescence, and nutrient recycling.-J. Exp. Bot. 65: 3799-3811, 2014. Go to original source...
    3. Baena-González E., Rolland F., Thevelein J.M., Sheen J.: A central integrator of transcription networks in plant stress and energy signalling.-Nature 448: 938-943, 2007. Go to original source...
    4. Biswal B., Biswal U.C.: Leaf senescence: physiology and molecular biology.-Curr. Sci. India 77: 775-782, 1999.
    5. Biswal B., Joshi P.N., Raval M.K., Biswal U.C.: Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation.-Curr. Sci. India 101: 47-56, 2011.
    6. Biswal B., Mohapatra P.K., Raval M.K., Biswal U.C.: Photosynthetic regulation of senescence in green leaves: involvement of sugar signaling.-In: Itoh S., Mohanty P., Guruprasad K.N. (ed.): Photosynthesis: Overviews on Recent Progress and Future Prospectives. Pp. 245-260. IK International Publishing House, New Delhi 2012.
    7. Biswal B., Pandey J.K.: Development of chloroplast: biogenesis, senescence, and regulations.-In: Pessarakli M (ed.): Handbook of Photosynthesis, 3rd ed. Pp. 77-93. CRC Press, Boca Raton 2016. Go to original source...
    8. Biswal U.C., Basanti B., Raval M.K.: Chloroplast Biogenesis: from Proplastid to Gerontoplast. Pp. 353. Kluwer Academic Publishers, Dordrecht 2003. Go to original source...
    9. Breeze E., Harrison E., McHattie S. et al.: High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation.-Plant Cell 23: 873-894, 2011. Go to original source...
    10. Brummell D.A., Dal Cin V., Crisosto C.H., Labavitch J.M.: Cell wall metabolism during maturation, ripening and senescence of peach fruit.-J. Exp. Bot. 55: 2029-2039, 2004. Go to original source...
    11. Buchanan-Wollaston V., Page T., Harrison E. et al.: Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis.-Plant J. 42: 567-585, 20
    12. Carrión C.A., Martínez D.E., Costa M.L., Guiamet J.J.: Senescence-associated vacuoles, a specific lytic compartment for degradation of chloroplast proteins?-Plants 3: 498-512, 2014. Go to original source...
    13. Chrost B., Daniel A., Krupinska K.: Regulation of α-galactosidase gene expression in primary foliage leaves of barley (Hordeum vulgare L.) during dark-induced senescence.-Planta 218: 886-889, 2004. Go to original source...
    14. Costa M.L., Martínez D.E., Gomez F.M. et al.: Chloroplast protein degradation: involvement of senescence-associated vacuoles.-In: Biswal B., Krupinska K., Biswal U.C. (ed.): Plastid Development in Leaves during Growth and Senescence. Pp. 417-433. Springer, Dordrecht 2013. Go to original source...
    15. Fischer A.M.: The complex regulation of senescence.-Crit. Rev. Plant Sci. 31: 124-147, 2012. Go to original source...
    16. Franková L., Fry S.C.: Biochemistry and physiological roles of enzymes that 'cut and paste' plant cell-wall polysaccharides.-J. Exp. Bot. 64: 3519-3550, 2013. Go to original source...
    17. Fujiki Y., Nakagawa Y., Furumoto T. et al.: Response to darkness of late-responsive dark-inducible genes is positively regulated by leaf age and negatively regulated by calmodulinantagonist-sensitive signalling in Arabidopsis thaliana.-Plant Cell Physiol. 46: 1741-1746, 20 Go to original source...
    18. Fujiki Y., Yoshikawa Y., Sato T. et al.: Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars.-Physiol. Plantarum 111: 345-352, 2001. Go to original source...
    19. Gepstein S., Sabehi G., Carp M.-J. et al.: Large-scale identification of leaf senescence-associated genes.-Plant J. 36: 629-642, 2003. Go to original source...
    20. Gregersen P.L., Foyer C.H., Krupinska K.: Photosynthesis and leaf senescence as determinants of plant productivity.-In: Kumlehn J., Stein N. (ed.): Biotechnological Approaches to Barley Improvement. Pp. 113-138. Springer, Berlin-Heidelberg 2014. Go to original source...
    21. Gunawardena A.H., Greenwood J.S., Dengler N.G.: Cell wall degradation and modification during programmed cell death in lace plant, Aponogeton madagascariensis (Aponogetonaceae).-Am. J. Bot. 94: 1116-1128, 2007. Go to original source...
    22. Guo Y., Gan S.-S.: Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments.-Plant Cell Environ. 35: 644-655, 2012. Go to original source...
    23. Havé M., Marmagne A., Chardon F., Masclaux-Daubresse C.: Nitrogen remobilisation during leaf senescence: lessons from Arabidopsis to crops.-J. Exp. Bot. 68: 2513-2529, 2017. Go to original source...
    24. Hörtensteiner S., Feller U.: Nitrogen metabolism and remobilization during senescence.-J. Exp. Bot. 53: 927-937, 2002. Go to original source...
    25. Jamar C., du Jardin P., Fauconnier M.-L.: Cell wall polysaccharides hydrolysis of malting barley (Hordeum vulgare L.): a review.-Biotechnol. Agron. Soc. 15: 301-313, 2011.
    26. Joshi P., Nayak L., Misra A.N., Biswal B.: Response of mature, developing and senescing chloroplasts to environmental stress.-In: Biswal B., Krupinska K., Biswal U.C. (ed.): Plastid Development in Leaves during Growth and Senescence. Pp. 641-668. Springer, Dordrecht 2013. Go to original source...
    27. Kabbage M., Kessens R., Bartholomay L.C., Williams B.: The life and death of a plant cell.-Annu. Rev. Plant Biol. 68: 375-404, 2017. Go to original source...
    28. Kim J., Woo H.R., Nam H.G.: Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research.-Mol. Plant. 9: 813-825, 2016. Go to original source...
    29. Lee E.-J., Koizumi N., Sano H.: Identification of genes that are up-regulated in concert during sugar depletion in Arabidopsis.-Plant Cell Environ. 27: 337-345, 20
    30. Lee E.-J., Matsumura Y., Soga K. et al.: Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis.-Plant Cell Physiol. 48: 405-413, 20
    31. Li L., Sheen J.: Dynamic and diverse sugar signaling.-Curr. Opin. Plant Biol. 33: 116-125, 2016. Go to original source...
    32. Li Z., Zhao Y., Liu X. et al: LSD 2.0: an update of the leaf senescence database.-Nucleic Acids Res. 42: D1200-D1205, 2013. Go to original source...
    33. Lichtenthaler H.K.: Plastoglobuli, thylakoids, chloroplast structure and development of plastids.-In: Biswal B., Krupinska K., Biswal U.C. (ed.): Plastid Development in Leaves during Growth and Senescence. Pp. 337-361. Springer, Dordrecht 2013. Go to original source...
    34. Lim P.O., Kim H.J., Nam H.G.: Leaf senescence.-Annu. Rev. Plant Biol. 58: 115-136, 2007. Go to original source...
    35. Liu X., Li Z., Jiang Z. et al.: LSD: a leaf senescence database.-Nucleic Acids Res. 39: D1103-D1107, 2010. Go to original source...
    36. Minic Z.: Physiological roles of plant glycoside hydrolases.-Planta 227: 723-740, 2008. Go to original source...
    37. Mohapatra P.K., Patro L., Raval M.K. et al.: Senescence-induced loss in photosynthesis enhances cell wall β-glucosidase activity.-Physiol. Plantarum 138: 346-355, 2010. Go to original source...
    38. Moreira L.R.S., Milanezi N.G., Filho E.X.F.: Enzymology of plant cell wall breakdown: an update.-In: Buckeridge M.S., Goldman G.H. (ed.): Routes to Cellulosic Ethanol. Pp. 73-96. Springer, New York 2011. Go to original source...
    39. Ohsumi Y.: Historical landmarks of autophagy research.-Cell Res. 24: 9-23, 2014. Go to original source...
    40. Ono Y., Wada S., Izumi M. et al.: Evidence for contribution of autophagy to rubisco degradation during leaf senescence in Arabidopsis thaliana.-Plant Cell Environ. 36: 1147-1159, 20 Go to original source...
    41. Pandey J.K., Dash S.K., Biswal B.: Loss in photosynthesis during senescence is accompanied by an increase in the activity of β-galactosidase in leaves of Arabidopsis thaliana: modulation of the enzyme activity by water stress.-Protoplasma 254: 1651-1659, 2017a. Go to original source...
    42. Pandey J.K., Dash S.K., Biswal B.: Nitrogen-deficiency-induced loss in photosynthesis and modulation of β-galactosidase activity during senescence of Arabidopsis leaves.-Acta Physiol. Plant. 39: 75, 2017b. Go to original source...
    43. Patro L.: Water stress induced alterations in photosynthesis and activity of enzyme(s) associated with the breakdown of cell wall polysaccharides.-PhD Thesis, Sambalpur University, India 2012.
    44. Patro L., Mohapatra P.K., Biswal U.C., Biswal B.: Dehydration induced loss of photosynthesis in Arabidopsis leaves during senescence is accompanied by the reversible enhancement in the activity of cell wall β-glucosidase.-J. Photoch. Photobio. B 137: 49-54. 2014. Go to original source...
    45. Pourtau N., Jennings R., Pelzer E. et al.: Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis.-Planta 224: 556-568, 20
    46. Pourtau N., Marès M., Purdy S. et al.: Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence.-Planta 219: 765-772, 2004. Go to original source...
    47. Quirino B.F., Noh Y.-S., Himelblau E., Amasino R.M.: Molecular aspects of leaf senescence.-Trends Plant Sci. 5: 278-282, 2000. Go to original source...
    48. Rolland F., Baena-Gonzalez E., Sheen J.: Sugar sensing and signaling in plants: conserved and novel mechanisms.-Annu. Rev. Plant Biol. 57: 675-709, 2006. Go to original source...
    49. Sabater B., Martín M.: Chloroplast control of leaf senescence.-In: Biswal B., Krupinska K., Biswal U.C. (ed.): Plastid Development in Leaves during Growth and Senescence. Pp. 529-550. Springer, Dordrecht 2013. Go to original source...
    50. Sarwat M.: Leaf senescence in plants: nutrient remobilization and gene regulation.-In: Sarwat M., Ahmad A., Abdin M.Z., Ibrahim M.M. (ed.): Stress Signaling in Plants: Genomics and Proteomics Perspective, Vol. 2. Pp. 301-316. Springer International Publishing, Cham 2017. Go to original source...
    51. Schippers J.H.M.: Transcriptional networks in leaf senescence.-Curr. Opin. Plant Biol. 27: 77-83, 2015. Go to original source...
    52. Tonini P.P., Lisboa C.G.S., Silva C.O. et al.: Testa is involved in the control of storage mobilisation in seeds of Sesbania virgata (Cav.) Pers., a tropical legume tree from of the Atlantic Forest.-Trees 21: 13-21, 2007. Go to original source...
    53. van Doorn W.G.: Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels?-J. Exp. Bot. 59: 1963-1972, 2008. Go to original source...
    54. Wingler A., Purdy S., MacLean J.A., Pourtau N.: The role of sugars in integrating environmental signals during the regulation of leaf senescence.-J. Exp. Bot. 57: 391-399, 2006. Go to original source...
    55. Wingler A., Roitsch T.: Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses.-Plant Biol. 10: 50-62, 2008. Go to original source...
    56. Wolf S., Hématy K., Höfte H.: Growth control and cell wall signaling in plants.-Annu. Rev. Plant Biol. 63: 381-407, 2012. Go to original source...
    57. Xie Q., Michaeli S., Peled-Zehavi H., Galili G.: Chloroplast degradation: one organelle, multiple degradation pathways.-Trends Plant Sci. 20: 264-265, 2015. Go to original source...

    Return to the content