Home LiteratureArticle Details
PMID: 21870204 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Comparative spatiotemporal analysis of root aerenchyma formation processes in maize due to sulphate, nitrate or phosphate deprivation.

Protoplasma ·Vol. 249 ·No. 3 ·2012-07-00 ·Pages 671-86

Siyiannis VF, Protonotarios VE, Zechmann B, Chorianopoulou SN, Müller M, Hawkesford MJ, Bouranis DL

Abstract

Nitrate (N), phosphate (P) or sulphate (S) deprivation causes aerenchyma formation in maize (Zea mays L.) nodal roots. The exact mechanisms that trigger the formation of aerenchyma under these circumstances are unclear. We have compared aerenchyma distribution across the nodal roots of first whorl (just emerging in 10-day-old seedlings), which were subject to S, N or P deprivation over a period of 10 days in connection with oxygen consumption, ATP concentration, cellulase and polygalacturonase activity in the whole root. The effect of deprivation on aerenchyma formation was examined using light and electron microscopy, along with in situ detection of calcium and of reactive oxygen species (ROS) by fluorescence microscopy. Aerenchyma was not found in the root base regardless of the deprivation. Programmed cell death (PCD) was observed near the root tip, either within the first two days (-N) or a few days later (-S, -P) of the treatment. Roots at day 6 under all three nutrient-deprived conditions showed signs of PCD 1 cm behind the cap, whereas only N-deprived root cells 0.5 cm behind the cap showed severe ultrastructural alterations, due to advanced PCD. The lower ATP concentration and the higher oxygen consumptions observed at day 2 in N-, P- and S-deprived roots compared to the control indicated that PCD may be triggered by perturbations in energy status of the root. The peaks of cellulase activity located between days 3 (-N) and 6 (-P), along with the respective alterations in polygalacturonase activity, indicated a coordination which preceded aerenchyma formation. ROS and calcium seemed to contribute to PCD initiation, with ROS possessing dual roles as signals and eliminators. All the examined parameters presented both common features and characteristic variations among the deprivations.

MeSH Terms
Adenosine Triphosphate/metabolism Autophagy Calcium/metabolism Cellulase/metabolism DNA, Plant/metabolism Energy Metabolism Nitrates/metabolism Oxygen Consumption Phosphates/metabolism Plant Proteins/metabolism Plant Roots/growth & development,metabolism,ultrastructure Polygalacturonase/metabolism RNA, Plant/metabolism Reactive Oxygen Species/metabolism Sulfates/metabolism Zea mays/growth & development,metabolism
Chemicals
DNA, Plant Nitrates Phosphates Plant Proteins RNA, Plant Reactive Oxygen Species Sulfates Adenosine Triphosphate Polygalacturonase Cellulase Calcium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Siyiannis Vassilis F
Plant Physiology Laboratory, Plant Biology Department, Faculty of Agricultural Biotechnology, Agricultural University of Athens, 75 Iera Odos, 11855, Athens, Greece.
Protonotarios Vassilis E
Zechmann Bernd
Chorianopoulou Styliani N
Müller Maria
Hawkesford Malcolm J
Bouranis Dimitris L
References (30)
30 references, click to expand
  1. Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).
    Planta. 2001 Jan;212(2):205-14 PMID: 11216841
  2. The mitochondrial permeability transition pore and its role in cell death.
    Biochem J. 1999 Jul 15;341 ( Pt 2):233-49 PMID: 10393078
  3. Abiotic stress signal transduction in plants: Molecular and genetic perspectives.
    Physiol Plant. 2001 Jun;112(2):152-166 PMID: 11454221
  4. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes.
    Ann Bot. 2004 Apr;93(4):359-68 PMID: 14980975
  5. Dynamics of Aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize.
    Ann Bot. 2006 May;97(5):695-704 PMID: 16481362
  6. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
    Plant Cell. 1998 Feb;10(2):255-66 PMID: 9490748
  7. Death proteases come alive.
    Trends Plant Sci. 2004 Oct;9(10):469-72 PMID: 15465679
  8. The role of calcium in oligogalacturonide-activated signalling in soybean cells.
    Planta. 2002 Aug;215(4):596-605 PMID: 12172842
  9. Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.
    Plant Physiol. 1989 Sep;91(1):266-71 PMID: 16667008
  10. Specialized zones of development in roots.
    Plant Physiol. 1995;109:725-7 PMID: 11539165
  11. Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability.
    Ann Bot. 2011 Apr;107(5):829-41 PMID: 20971728
  12. Control of plant development by reactive oxygen species.
    Plant Physiol. 2006 Jun;141(2):341-5 PMID: 16760485
  13. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?
    Trends Plant Sci. 2000 May;5(5):225-30 PMID: 10785669
  14. Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses.
    Plant Physiol. 2005 Oct;139(2):566-73 PMID: 16219918
  15. How plants make tubes.
    Trends Plant Sci. 2003 Apr;8(4):159-64 PMID: 12711227
  16. Transduction of an Ethylene Signal Is Required for Cell Death and Lysis in the Root Cortex of Maize during Aerenchyma Formation Induced by Hypoxia.
    Plant Physiol. 1996 Oct;112(2):463-472 PMID: 12226403
  17. Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium.
    Plant Physiol. 2011 Jul;156(3):1190-201 PMID: 21628631
  18. Mitochondria as ATP consumers: cellular treason in anoxia.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8670-4 PMID: 10890886
  19. Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage.
    Planta. 1983 Jul;157(4):350-7 PMID: 24264269
  20. Mannose induces an endonuclease responsible for DNA laddering in plant cells.
    Plant Physiol. 1999 Sep;121(1):71-80 PMID: 10482662
  21. Monitoring reactive oxygen species formation and localisation in living cells by use of the fluorescent probe CM-H(2)DCFDA and confocal laser microscopy.
    Physiol Plant. 2009 Aug;136(4):369-83 PMID: 19493304
  22. Impact of oxygen stress and energy availability on membrane stability of plant cells.
    Ann Bot. 2002 Oct;90(4):499-507 PMID: 12324274
  23. Aerenchyma formation in roots of maize during sulphate starvation.
    Planta. 2003 Jul;217(3):382-91 PMID: 12728316
  24. Intracellular adaptations of glutathione content in Cucurbita pepo L. induced by treatment with reduced glutathione and buthionine sulfoximine.
    Protoplasma. 2006 May;227(2-4):197-209 PMID: 16520878
  25. The role of the distal elongation zone in the response of maize roots to auxin and gravity.
    Plant Physiol. 1993 Aug;102(4):1203-10 PMID: 11536543
  26. Effect of inorganic phosphate concentration on the nature of inner mitochondrial membrane alterations mediated by Ca2+ ions. A proposed model for phosphate-stimulated lipid peroxidation.
    J Biol Chem. 1996 Feb 9;271(6):2929-34 PMID: 8621682
  27. Plant vacuoles
    Plant Cell. 1999 Apr;11(4):587-600 PMID: 10213780
  28. On the voltage dependence of the mitochondrial permeability transition pore. A critical appraisal.
    J Biol Chem. 1997 May 9;272(19):12295-9 PMID: 9139672
  29. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy.
    Biochim Biophys Acta. 1998 Aug 10;1366(1-2):177-96 PMID: 9714796
  30. Programmed cell death and aerenchyma formation in roots.
    Trends Plant Sci. 2000 Mar;5(3):123-7 PMID: 10707078
Article Info
Journal
Protoplasma
Abbr.
Protoplasma
ISSN
1615-6102
Published
2012-07-00
Epub
2011-00-26
Pages
671-86
Language
English
Region
Austria
NLM ID
9806853
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com