Aerenchyma formation in crop species: A review

Flooding is a major problem in many crop areas around the world. However, many wetland plant species can expand their roots into flooded soils because of the presence of longitudinal aerenchyma channels that facilitate oxygen diffusion from the shoots to the root tips. Aerenchyma also forms in rice roots, allowing rice plants to grow well in flooded paddy fields. Aerenchyma formation therefore helps plants to survive flooding. “Primary aerenchyma” forms in the roots of some cereal crops such as rice, maize, barley and wheat. “Secondary aerenchyma” forms in the stem, hypocotyl, tap root, adventitious roots, and root nodules of some legume crops such as soybean. This paper reviews the recent progress in the study of aerenchyma formation, and highlights the role that primary aerenchyma in cereal crops and secondary aerenchyma in soybean can play in improving their tolerance to flooding.

[1]  M. Drew,et al.  Ethylene Biosynthesis during Aerenchyma Formation in Roots of Maize Subjected to Mechanical Impedance and Hypoxia , 1996, Plant physiology.

[2]  A. Arber.  Water Plants; A Study of Aquatic Angiosperms , 2008 .

[3]  P. A. Attwood,et al.  Roots of willow (Salix viminalis L.) show marked tolerance to oxygen shortage in flooded soils and in solution culture , 1996, Plant and Soil.

[4]  M. Nakazono,et al.  Mechanisms for coping with submergence and waterlogging in rice , 2012, Rice.

[5]  T. Mochizuki,et al.  Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean (Glycine max) under flooded conditions , 2003, Plant and Soil.

[6]  Y. Mano,et al.  High-density linkage map around the root aerenchyma locus Qaer1.06 in the backcross populations of maize Mi29 × teosinte “Zea nicaraguensis” , 2009 .

[7]  T. Colmer,et al.  Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. , 2003, Functional plant biology : FPB.

[8]  D. Mcpherson,et al.  CORTICAL AIR SPACES IN THE ROOTS OF ZEA MAYS L. , 1939 .

[9]  B. Benz,et al.  Zea nicaraguensis (Poaceae), a new teosinte from Pacific Coastal Nicaragua. , 2000 .

[10]  Thomas Geske,et al.  Aerenchyma formation in the rice stem and its promotion by H2O2. , 2011, The New phytologist.

[11]  H. Greenway,et al.  Tolerance of wheat (Triticum aestivum cvs Gamenya and Kite) and triticale (Triticosecale cv. Muir) to waterlogging , 1992 .

[12]  F. Ponnamperuma,et al.  CHAPTER 2 – Effects of Flooding on Soils , 1984 .

[13]  Y. Mano,et al.  Verification of QTL controlling root aerenchyma formation in a maize × teosinte “Zea nicaraguensis” advanced backcross population , 2008 .

[14]  K. Shiono,et al.  Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. , 2011, Annals of botany.

[15]  H. Konings.  Ethylene‐promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non‐aerated conditions , 1982 .

[16]  Paul J Thornalley,et al.  Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. , 1985, Biochimica et biophysica acta.

[17]  G. Boru,et al.  Responses of soybean to oxygen deficiency and elevated root-zone carbon dioxide concentration. , 2003, Annals of botany.

[18]  M. Nakazono,et al.  Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species , 2011, Plant signaling & behavior.

[19]  T. Mochizuki,et al.  Secondary Aerenchyma Formation and its Relation to Nitrogen Fixation in Root Nodules of Soybean Plants (Glycine max) Grown under Flooded Conditions , 2002 .

[20]  R. Dudal.  Inventory of the major soils of the world with special reference to mineral stress hazards. , 1976 .

[21]  T. Setter,et al.  Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats , 2003, Plant and Soil.

[22]  C. R. Metcalfe.  The "Aerenchyma" of Sesbania and Neptunia , 1931 .

[23]  A. Saxton,et al.  Response of Solid-Seeded Soybean to Flood Irrigation. II. Flood Duration , 1988 .

[24]  M. Drew,et al.  Transduction of an Ethylene Signal Is Required for Cell Death and Lysis in the Root Cortex of Maize during Aerenchyma Formation Induced by Hypoxia , 1996, Plant physiology.

[25]  H. D. Scott,et al.  Flood duration effects on soybean growth and yield , 1989 .

[26]  J. Dangl,et al.  Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. , 2005, Current opinion in plant biology.

[27]  H. Greenway,et al.  Conditions leading to high CO2 (>5 kPa) in waterlogged-flooded soils and possible effects on root growth and metabolism. , 2006, Annals of botany.

[28]  K. Shiono,et al.  Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. , 2011, The New phytologist.

[29]  T. Colmer,et al.  Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations. , 2006, The New phytologist.

[30]  M. Jackson,et al.  Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency , 1981, Planta.

[31]  R. E. Sojka,et al.  SOIL OXYGEN EFFECTS ON TWO DETERMINATE SOYBEAN ISOLINES1 , 1985 .

[32]  D. Sleper,et al.  Yield and nutritional responses to waterlogging of soybean cultivars , 2009, Irrigation Science.

[33]  H. Wager,et al.  On the Floating-Roots of Sesbania aculeata, Pers , 1888 .

[34]  T. Colmer.  Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots , 2003 .

[35]  K. Shiono,et al.  Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). , 2012, Plant, cell & environment.

[36]  W. Armstrong,et al.  Chlorophyll development in mature lysigenous and schizogenous root aerenchymas provides evidence of continuing cortical cell viability. , 1994, The New phytologist.

[37]  W. Armstrong,et al.  Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence , 1999 .

[38]  W. Armstrong.  Aeration in Higher Plants , 1980 .

[39]  D. Evans,et al.  Aerenchyma formation: Tansley review , 2003 .

[40]  S. Guerreiro,et al.  Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. , 2005, Annals of botany.

[41]  M. Sachs,et al.  Molecular and cellular adaptations of maize to flooding stress. , 2003, Annals of botany.

[42]  T. Colmer,et al.  Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids. , 2011, The New phytologist.

[43]  E. Visser,et al.  Aerenchyma formation in the wetland plant Juncus effusus is independent of ethylene. , 2006, The New phytologist.

[44]  N. Suzuki,et al.  Respiratory burst oxidases: the engines of ROS signaling. , 2011, Current opinion in plant biology.

[45]  M. Jackson,et al.  Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize ( Zea mays L.) promoted by ethylene , 2001 .

[46]  M. Drew,et al.  Programmed cell death and aerenchyma formation in roots. , 2000, Trends in plant science.

[47]  C. Blom.  Adaptations to Flooding Stress: From Plant Community to Molecule , 1999 .

[48]  J. Board,et al.  Waterlogging effects on growth and yield components in late-planted soybean. , 1998, Crop science.

[49]  M. Jackson,et al.  Physiology, Biochemistry and Molecular Biology of Plant Root Systems Subjected to Flooding of the Soil , 2003 .

[50]  S. Komatsu,et al.  Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. , 2010, Annals of botany.

[51]  W. Armstrong.  Oxygen Diffusion from the Roots of Woody Species , 1968 .

[52]  K. Shimamoto,et al.  Down-Regulation of Metallothionein, a Reactive Oxygen Scavenger, by the Small GTPase OsRac1 in Rice , 2004, Plant Physiology.

[53]  M. Jackson,et al.  Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen , 1985, Planta.

[54]  Pieter Verboven,et al.  Root aeration via aerenchymatous phellem: three-dimensional micro-imaging and radial O2 profiles in Melilotus siculus. , 2012, The New phytologist.

[55]  S. Davis.  Allocation to floral structures in Thalictrum pubescens (Ranunculaceae), a cryptically dioecious species. , 2002, Annals of botany.

[56]  M. Sachs,et al.  Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. , 1994, The Plant cell.

[57]  J. Sprent,et al.  Surface features of soybean root nodules , 1975, Protoplasma.

[58]  H. Daimon,et al.  Histological observation of secondary aerenchyma formed immediately after flooding in Sesbania cannabina and S. rostrata , 2003 .

[59]  M. Drew,et al.  The Development of Waterlogging Damage in Young Wheat Plants in Anaerobic Solution Cultures , 1980 .

[60]  H. Araki.  Water uptake of soybean (Glycine max L. Merr.) during exposure to O2 deficiency and field level CO2 concentration in the root zone , 2006 .

[61]  J. Kuo,et al.  Nitrogen Fixation by Nodulated Roots of Viminaria juncea (Schrad. & Wendl.) Hoffmans, (Fabaceae) When Submerged in Water , 1983 .

[62]  B. Kindiger,et al.  QTL mapping of root aerenchyma formation in seedlings of a maize × rare teosinte “Zea nicaraguensis” cross , 2007, Plant and Soil.

[63]  E. Barrett-Lennard,et al.  Aerenchymatous phellem in hypocotyl and roots enables O2 transport in Melilotus siculus. , 2011, The New phytologist.

[64]  K. Stevens,et al.  The aerenchymatous phellem of Lythrum salicaria (L.): a pathway for gas transport and its role in flood tolerance. , 2002, Annals of botany.

[65]  R. Parsons,et al.  Mechanism of soybean nodule adaptation to different oxygen pressures , 1990 .

[66]  M. Sauter,et al.  Epidermal Cell Death in Rice Is Confined to Cells with a Distinct Molecular Identity and Is Mediated by Ethylene and H2O2 through an Autoamplified Signal Pathway[W] , 2009, The Plant Cell Online.

[67]  N. Galwey,et al.  Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss , 2001 .

[68]  R. Bird,et al.  QTL mapping of above-ground adventitious roots during flooding in maize x teosinte "Zea nicaraguensis" backcross population , 2009 .

[69]  M. Sachs,et al.  A Flooding-Induced Xyloglucan Endo-Transglycosylase Homolog in Maize Is Responsive to Ethylene and Associated with Aerenchyma , 1996, Plant physiology.

[70]  J. Sekiya,et al.  Nitrogen Fixation of Sesbania rostrata : Contribution of Stem Nodules to Nitrogen Acquisition , 1992 .

[71]  J. Pires,et al.  Adaptações morfofisiológicas da soja em solo inundado , 2002 .

[72]  K. Dittert,et al.  Responses of Alnus glutinosa to anaerobic conditions--mechanisms and rate of oxygen flux into the roots. , 2006, Plant biology.

[73]  Guodong Yang,et al.  Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast , 2008, Journal of experimental botany.

[74]  M. Jackson,et al.  Aerenchyma (Gas-space) Formation in Adventitious Roots of Rice (Oryza sativa L.) is not Controlled by Ethylene or Small Partial Pressures of Oxygen , 1985 .

[75]  G. Stephenson,et al.  Morphological and Anatomical Responses of Lythrum salicaria L. (Purple Loosestrife) to an Imposed Water Gradient , 1997, International Journal of Plant Sciences.