Programmed cell death and aerenchyma formation in roots

doi:10.1016/S1360-1385(00)01570-3

Trends in Plant Science

Volume 5, Issue 3, 1 March 2000, Pages 123-127

https://doi.org/10.1016/S1360-1385(00)01570-3 Get rights and content

Abstract

Lysigenous aerenchyma contributes to the ability of plants to tolerate low-oxygen soil environments, by providing an internal aeration system for the transfer of oxygen from the shoot. However, aerenchyma formation requires the death of cells in the root cortex. In maize, hypoxia stimulates ethylene production, which in turn activates a signal transduction pathway involving phosphoinositides and Ca²⁺. Death occurs in a predictable pattern, is regulated by a hormone (ethylene) and provides an example of programmed cell death.

Section snippets

Aerenchyma function

Lysigenous aerenchyma provides not only an internal pathway for O₂ transfer, but also simultaneously reduces the number of O₂-consuming cells, a feature that might assist in low O₂ environments. It has been suggested that aerenchymatous organs are often water- or fluid-filled⁵, a feature that would prevent them from functioning in O₂ transfer. However, evidence from the measurement of gas-filled porosity, microscopic observation (Fig. 1) and O₂ transport⁶ is overwhelming – the lacunae are

Induction of lysigenous aerenchyma

Hypoxia under laboratory conditions readily induces aerenchyma formation in the roots of maize (Fig. 2), and hypoxia probably accounts for the induction of aerenchyma in roots in flooded soils. Hypoxia might be a much more common occurrence within roots than has been supposed. Even in well- oxygenated surroundings, the rate of O₂ consumption during respiration, especially at warm temperatures, can outpace the rate of supply of O₂ to the respiring cells. Microsensors for O₂ have shown steep

Ethylene signal transduction pathway

Induction of cell death in the root cortex of maize has been examined in relation to the possible pathway downstream of ethylene²⁶. A variety of agonists and antagonists of particular steps in signal transduction have been used in this pharmacological approach. In well-oxygenated roots, cell death can be initiated by GTP-γ-S, which activates heterotrimeric G proteins. Death was also induced by okadaic acid (Fig. 2), which inhibits protein phosphatases, thereby tending to maintain proteins in a

Programmed cell death

Programmed cell death (PCD) can be defined as death resulting from the activation of a specific biochemical pathway that is under the genetic control of the cell, and therefore it amounts to cellular suicide30, 31. Apoptosis is a particular form of PCD, which is defined in animal cells by a combination of changes. These include:

•
Nuclear condensation.
•
Activation of Ca²⁺-dependent endonucleases with DNA fragmentation into characteristic, internucleosomal lengths of 180–200 bp or multiples thereof.
•

Conclusions

Aerenchyma formation by cell death and lysigeny provides an ideal model system for examining the initiation of PCD by environmental factors or by the phytohormone, ethylene. Information is accumulating on the signal transduction pathway, only parts of which may have features in common with that in Arabidopsis. A rise in cytosolic Ca²⁺ and rupture of the tonoplast are early events common to death of TEs and root cortical cells, and it will be interesting to explore the similarities between these

Acknowledgements

Research on aerenchyma formation in M.C.D.’s and P.M.W.’s laboratories is supported by a competitive grant from the US Dept of Agriculture, National Research Initiative program.

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Trends in Plant Science

ReviewProgrammed cell death and aerenchyma formation in roots

Abstract

Section snippets

Aerenchyma function

Induction of lysigenous aerenchyma

Ethylene signal transduction pathway

Programmed cell death

Conclusions

Acknowledgements

Ann. Bot.

Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae)

Am. J. Bot.

Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage

Planta

Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots

Planta

Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae)

Am. J. Bot.

Apoplastic water and solute movement: new rules for an old space

Annu. Rev. Plant Physiol. Plant Mol. Biol.

Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia

Annu. Rev. Plant Physiol. Plant Mol. Biol.

Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L

Plant Physiol.

Induction of enzymes associated with lysigenous aerenchyma formation in roots of Zea mays during hypoxia or nitrogen-starvation

Plant Physiol.

Root aerenchyma development in Spartina patens in relation to flooding

Am. J. Bot.

The anatomical characteristics of roots and plant response to soil flooding

New Phytol.

Introgressing root aerenchyma into maize

Maydica

Aerenchyma (gas-space) formation in adventitious roots of rice (Oryza sativa L) is not controlled by ethylene or small partial pressures of oxygen

J. Exp. Bot.

Eastern gamagrass (Tripsacum dactyloides) root penetration into and chemical properties of claypan soils

Plant Soil

Ethylene biosynthesis during aerenchyma formation in roots of Zea mays subjected to mechanical impedance and hypoxia

Plant Physiol.

Soybean root morphological and anatomical traits associated with acclimation to flooding

Crop Sci.

Survival tactics of Ranunculus species in river floodplains

Oecologia

Review
Programmed cell death and aerenchyma formation in roots