7 Root Oxygen Deprivation and the 1 Reduction of Leaf Stomata) Aperture and Gas Exchange Robert E. Sojka Northwest Irrigation and Soils Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture Derrick M. Oosterhuis Department of Crops, Soils, and Environmental Sciences, University of Arkansas H. Don Scott Center for Agribusiness and Environmental Policy, Mount Olive Col lege CONTENTS 1. Introduction 299 Flooding and Hypoxia Effects on Soil Processes 300 Soil Hypoxia, the Rhizosphere, and Plant Metabolism 302 IV. Hypoxia and Stomata] Closure 302 V. Stomata Closure Mechanisms 307 VI. Summary 308 References 308 I. INTRODUCTION transpiration and the complex system of hormonal control of plant systems and processes. The most ubiquitous plant abiotic stress in the global Figure 17.1 gives a conceptual diagram of the environment is generally thought to be water deficit. effects of flooding on the yield potential of a crop The opposite of water-deficit stress. flooding, initially and compares the pattern with what is typically seen involves relief of the abiotic factor of water deficit and under drought. With drought stress, onset is very only becomes stressful after flooding persists long gradual and plant adaptation has ample time to enough to directly or indirectly interfere with a var- occur at a pace that moderates the impact of the iety of plant functions via several mechanisms. The water-deficit stress. Drought would have to persist relief of stress with short term flooding (typically a for weeks in most crops to collapse the yield potential day or less) is the principle upon which irrigation to near-zero levels. Unless water-deficit stress is ex- hinges. By contrast, the negative impacts of pro- ceedingly severe and has persisted for weeks, the loss longed flooding on ecosystems, and particularly agri- in yield potential is moderate, and relief of the stress cultural production systems, are substantial [I] and can usually bring about substantial recovery in yield may be as significant as drought, depending on one's potential. even full recovery, although yield compon- accounting strategy. Much of this impact is the result ents may shift. By contrast, when flooding occurs, of the combination of soil and plant chemical, phys- plants initially see relief of any water deficit stress ical, and biological changes that cause stomata to they may be experiencing. However, as the oxygen close after prolonged flooding. This contributes sig- in the root zone is depleted by plant roots and com- nificantly to a drastic reduction in photosynthesis and peting soil organisms (usually in the first 24-48 h), the damages many other plant functions by disrupting initial boost in yield potential rapidly gives way to a 299 300 Handbook of Photosynthesis Stress initiation Drought Flood Stress relief FIGURE 17.1 Conceptual comparison of stress accumu- lation and stress relief effect on yield potential for flood- ing stress vs. drought stress. Days precipitous drop. Stress relief upon drainage typically affect soil mineral and biological processes. Ponnam- produces a far more gradual, and usually less success- peruma [12] gave an excellent summary of the physi- ful recovery than with moderate drought, simply be- cochemical processes that occur in soil upon cause the plant infrastructure is often far more prolonged flooding, depleting oxygen as an electron devastated by the many system impairments that acceptor. As reactive oxygen disappears, soil redox can accumulate with flooding. In our chapter, refer- potential falls, causing a cascading series of organic ence to flooding in the context of this subject matter and mineral transformations, resulting in the release refers to prolonged flooding, typically 24-48 h or of numerous soluble chemically reduced minerals, longer, which is about the length of time usually many of which are toxic to plants including methane, needed for soil organisms to deplete soil water of sulfides, and reduced forms of iron and manganese. dissolved oxygen. Water is essential to most soil biological activities. It is interesting and curious that common plant As the amount of water in the soil environment shifts reactions to root inundation or prolonged flooding from shortage to plentiful and on to excess, the popu- involve several physiological responses much akin to lations and functional dominance of competing or- drought stress. This occurs even thou gh plant roots ganisms also shift. Under excessively wet or flooded are submerged, i.e.. in contact with free water. That conditions, disease organisms are often favored [8]. wilting and stomatal closure occuring in flooded Water affects the heat capacity, heat conductivity, plants indicate that the physiological responses to and evaporative properties of soil in a way that gen- flooding are not caused by the energy status of the erally tends to cool soil when wet. Water is a potent water, which is the dominant direct mechanism initi- solvent, facilitating the mobility of mineral and or- ating wilting and stomatal closure during drought. ganic solutes, to the benefit or detriment of a given The physiological responses to soil hypoxia and soil biological process, depending on the intensity and flooding have been reviewed by a number of scientists direction of solute movement into or out of an organ- [I-5]. ism's sphere of influence. The wilting, stomatal closure, and various other Very important to our discussion is the fact that physiological responses to flooding have been water also changes the net oxygen availability of the explained by several plant response scenarios. These soil environment in a temperature-dependent fashion. fall into about five categories: obstruction of xylem While soil aeration can be characterized as the vol- elements by disease organisms, reduced root system ume of gas-filled pore space in a given soil volume, or extent or root system/membrane water conductance, as the concentration of oxygen (and other gases) altered soil—plant nutritional status, production or within the pores, most edaphologists agree that soil imbalancing of plant hormones or biochemical sig- oxygen diffusion rate (ODR) is the best indicator of naling compounds, and the action of soil- or plant- soil aeration status. This is because ODR gives an produced toxins [2,6-11]. indication of the soil's ability to supply oxygen to organisms as a rate function [13]. Rhizosphere ODR is also relatively easy to determine using the platinum II. FLOODING AND HYPDXIA EFFECTS ON microeIectrode technique [14,15], and leaves both soil SOIL PROCESSES and roots essentially undisturbed. The rate at which soil can supply oxygen must be balanced against the The way in which flooding or waterlogging proceeds rate at which an organism in soil consumes oxygen. along a given scenario or set of scenarios is related to This balance of rates has been the basis of under- how the physical and chemical properties of water standing and modeling soil-oxygen-mediated pro- Root Oxygen Deprivation 301 400 cascading chemical, biochemical, and physical pro- 293K Standard (=100%) cesses in the soil, rhizosphere, and the plant). Respiration rate Ow = 2 350 Our chapter focuses primarily on the role of root • Dau. 02014 ce/sec 02 zone hypoxia and anoxia in bringing about stomatal 300 D.wme,02 = 2.10 x10-' cm2kec closure. While flooding or waterlogging is certainly • qSC .0.03132 ml gas 250 at STRimi spin the most common circumstance limiting root oxygen availability, it is not the sole scenario. Several other 200 examples can be noted. Generous incorporation of 150 fresh organic matter into warm wet soil can stimulate cc depletion of soil oxygen through the respiration of 100 microorganisms decomposing the fresh substrate. Soil 50 compaction. which reduces average gas-filled soil pore size and total pore space of soil, creates many 10 15 20 25 30 35 40`C 0 dead-end soil pores, and favors blockage of the smal- 270 280 290 300 310 ler soil pores with water films, restricting diffusion of Temperature (K) oxygen through the soil matrix. Oxygen diminishes with soil depth, and if an established plant's roots are FIGURE 17.2 Relative temperature-related changes in corn buried too deeply under additional soil, the root sys- root respiration rate (assuming respiration rate doubles for tem can become oxygen limited. each 10 K increase, i.e., Q 10 2), diffusion coefficient (D) The dominant literature, of course, relates to of 02 in air and in water, and 0? solubility coefficient (OSC) in water. (From Ref. [9], as adapted from Refs. [17,18].) flooding; however, a number of studies have manipu- lated soil oxygen independently of flooding, providing important insights to the phenomena [8]. Also, since oxygen unavailability is probably the dominant direct cesses [16.17]. Luxrnoore and Stolz)/ [18] gave an trigger for most of the plant responses that ultimately elegant graphic depiction of this dependency (Figure manifest themselves as familiar visual and otherwise 17.2). easily monitored physiological responses. it is logical As soil water content increases. the thickness of to quantitatively tie measurable physiological re- water films around soil particles. microorganisms. sponses to rhizosphere ODR values. ODR can be and surfaces of plant roots also increases. The thick- physically predicted with reasonable reliability for a ness of these water films greatly influences the transfer range of soil conditions [26-28]. Thus, the correlation of oxygen from the soil environment to respiration of quantifiable physiological responses to ODR meas- sites in roots and microorganisms [8]. Oxygen diffuses urements facilitates the normalizing of responses to a 104 times more slowly through water than through air reliable soil indicator, allowing species and cultivar [19] and only one-fourth as rapidly through dense response comparisons. Ultimately this approach also protoplasm as through water [20,21]. The physics of enables modeling of physiological responses on a this process are described by Fick's first law: sound physical basis.