Flooding and Plant Growth

Abstract

This Special Issue is based on the 7th Conference of the International Society for Plant Anaerobiosis (ISPA), held in Nijmegen, The Netherlands, 12–16 June 2001. The papers describe and analyse many of the responses that plants display when subjected to waterlogging of the soil or deeper submergence. These responses may be injurious or adaptive, and are discussed at various levels of organizational complexity ranging from ecosystem processes, through individual plants to single cells. The research incorporates molecular biology and genetics, cell physiology, biochemistry, hormone physiology, whole plant physiology, plant demography and ecology. The study of the damage to young rice plants caused by submergence, especially as experienced in the rainfed lowlands of Asia, is comprehensively addressed. This work integrates various specialized approaches ranging from agronomy to molecular genetics, and demonstrates how plant biology can be harnessed to improve stress tolerance in an important crop species while simultaneously improving basic understanding of tolerance mechanisms and plant processes.

Received: 21 September 2002; Returned for revision: 4 October 2002; Accepted: 22 October 2002

INTRODUCTION

Flooding and submergence are major abiotic stresses and rank alongside water shortage, salinity and extreme temperatures as major determinants of species distribution worldwide. Success or failure of crops in much arable farmland can also be determined by the frequency and extent of flooding. The International Society for Plant Anaerobiosis (ISPA) has promoted and coordinated the study of plant responses to these stresses and other aspects of impeded plant aeration since its inception at the XII International Botanical Congress in Leningrad (now St Petersburg) in 1975. Since that time members of the ISPA have organized meetings, workshops and sessions on plant aeration at major scientific conferences on plant aeration in Russia (1975, 1985), UK (1985, 1993, 1995, 2001), USA (1986, 1999, 2000), Switzerland (1987), Iceland (1992), Japan (1993), Czechoslovakia (1994) and Finland (1995). Several of these meetings have resulted in books (Hook and Crawford, 1978; Crawford et al., 1987; Hook et al., 1988; Jackson et al., 1991; Jackson and Black, 1993; Crawford et al., 1994) and issues or part issues of journals [Annals of Botany74(3) 1994; 79 (Suppl. A) 1997; 86(3) 2000; 90(4) 2002]. These publications have helped to establish the study of plant life under flooding and submergence as a major topic in plant biology, incorporating some of the most progressive elements of botanical research. The current issue of Annals of Botany contains a selection of papers by speakers at the 7th and latest ISPA Conference, which was held at Nijmegen, The Netherlands, from 12 to 16 June 2001 and which attracted almost 100 delegates from Europe, Asia, Australia and North America. It was arranged under the aegis and patronage of the International Committee on Global Climate and Plant Environment Stresses. Support from The Royal Netherlands Academy of Arts and Sciences, Utrecht University, the University of Nijmegen, and The Royal Botanical Society of the Netherlands made the conference financially possible.

MAJOR TOPICS CONTAINED IN THIS SPECIAL ISSUE

Plants adapt to their ever‐changing environment in many ways, leading to a wealth of growth forms of varying complexity. Certain habitats demand exceptional adaptations, especially when one or more essential resources is scarce or absent. The conditions prevailing in wetlands are an example of such an extreme environment since the highly water‐saturated soils exclude oxygen, one of the fundamental requirements for plant life. Oxygen starvation in these soils arises from an imbalance between the slow diffusion of gases in water compared with air and the rate that oxygen is consumed by micro‐organisms and plant roots. The outcome is that flooded soil quickly becomes devoid of oxygen at depths below a few millimeters. In the floodwater itself, broad unstirred boundary layers quickly develop around respiring tissues. This alone can lead to tissue oxygen deficiency within a few hours. Since roots and rhizomes are essentially aerobic organs, the consequences can be fatal because, as aerobic respiration ceases, levels of energy‐rich adenylates drop rapidly, causing a dramatic decline in ion uptake and transport (Huang et al., 2003; Vartapetian et al., 2003). The variety of habitats in which occasional or regular flooding takes place is large, and some are currently increasing in area. This is certainly the case for the vast tundra that stretches from east Siberia via northern Europe to the north of the North American continent (Crawford et al., 2003).

Faced with oxygen depletion in the soil, plants have evolved a wide range of characteristic responses that appear to reduce the impact of the stress. Several of these acclimations can sometimes be found together. For example, plants may develop morphological and biochemical features that are either constitutive or are induced by the flooding event. Several anatomical responses facilitate internal transport of oxygen by diffusion or sometimes by mass flow. This permits underground organs to avoid developing anaerobic interiors. Of particular importance is the development of aerenchyma (gas‐filled channels that can interconnect throughout much of the plant). This creates a low resistance network for the transport of gases from well‐aerated aerial shoots to organs engulfed by anaerobic surroundings. The effectiveness of aerenchyma can be increased by the formation of gas‐tight barriers in the epidermis and exodermis in roots that inhibit radial loss of oxygen from roots to the surrounding oxygen‐deficient soil (Aschi‐Smiti et al., 2003; Colmer, 2003).

When floodwater deepens sufficiently to inundate the shoots as well as the roots, stress on the plants is much magnified. The extra stress arises because influx of aerial carbon dioxide for photosynthesis is largely prevented. Only a relatively small group of well‐adapted aquatic or amphibious species can survive total submergence of the shoot system for long at growing temperatures. The principal strategy for survival is to shorten the period of total submergence by means of a strong increase in the shoot elongation rate that reunites the shoot with air. In most cases this growth requires oxygen, is regulated by a build‐up of the plant hormone ethylene and is mediated via expression of expansin genes (Voesenek et al., 2003; Vriezen et al., 2003). In contrast, a small number of species (e.g. Potamogeton pectinatus) are also able to escape by means of accelerated vertical extension growth even in the complete absence of oxygen and independently of ethylene. Taken together, these acclimations help individual plants to survive through improved access to oxygen achieved by accelerated upward shoot growth.

Even species that are susceptible to poorly aerated conditions possess metabolic and molecular responses that lengthen survival time from a few hours to several days. All plant species synthesize so‐called anaerobic proteins that enable an oxygen‐independent energy‐generating metabolism to proceed where fermentable substrates are available (Subbaiah and Sachs, 2003). In better‐adapted species with large respirable reserves, these fermentation pathways can sustain survival under water for many months, and are the means by which aquatic perennials cope with seasonal winter flooding in cool latitudes. Particularly important is the fuelling of these fermentation processes. Soluble sugars are rapidly channelled to fermentative metabolism as soon as oxygen levels decrease. Since the amounts of these sugars are limited, starch breakdown is highly regulated by interactions between hormonal and sugar signals (Loreti et al., 2003). A further group of plants, typical of arctic regions, is able to withstand total anoxia for long periods, even as green plants (Crawford et al., 2003). This long‐term metabolic tolerance is seen as an adaptation to ice encasement or submergence in melt water that is common in artic regions, which comprise a fifth of the earth’s land surface. The mechanism may involve a highly controlled down‐regulation of almost all aspects of metabolism.

Prevention of the build‐up of potential phytotoxins is another mechanism that enhances plant survival under flooded conditions. A specific type of haemoglobin (phytoglobin) may play such a role by detoxifying nitric oxide formed during hypoxia of root tissues. Alternatively, phytoglobin may also regenerate NAD⁺, thereby serving as an alternative to fermentation as a source (Dordas et al., 2003). Reactive oxygen species (ROS) are possible phytotoxins affecting flooded plants. Low oxygen concentrations and the re‐oxygenation that occurs upon retreat of floodwater together favour the generation of ROS. Protection mechanisms against ROS involving chemical and enzymic antioxidant systems are essential traits of flood‐tolerant plants (Blokhina et al., 2003), helping to protect lipids and other macromolecules from oxidative damage.

As in most other areas of biological research, the development of new analytical tools has advanced our knowledge of detailed cellular processes considerably. The use of anaerobic promoters and histochemically detectable reporter genes is helping to dissect the signal transduction pathway involved in sensing and relaying the oxygen deficiency signal. For example, expression of a gene coding for glyceraldehyde‐3‐phosphate dehydrogenase, a glycolytic enzyme induced anaerobically in roots, leaves, stems and flowers of Arabidopsis thaliana is dependent on light and the substitution of oxygen with carbon dioxide (Hänsch et al., 2003). More novel genes involved in anaerobic signalling have been isolated in arabidopsis by Baxter‐Burrell et al. (2003) using two genetically engineered transposable DNA elements as mutagens. This screen has yielded genes not previously implicated in responses to oxygen deprivation, such as a putative receptor‐like kinase and a putative sensor‐histidine kinase. Other recent approaches, such as DNA chip technology and proteome analysis, are also helping to explore unknown (functions of) genes and proteins involved in adaptation to flooding and anaerobiosis (Dolferus et al., 2003). However, significant technical progress has not been restricted to the study of molecular genetics. Marked advances in quantitative methods for the trace analysis of metabolites produced during flooding have also been made using highly sensitive techniques such as photoacoustic spectroscopy (Boamfa et al., 2003). This equipment allows tracking the onset of anoxic processes such as fermentation with impressive time resolution and sensitivity.

Rice (Oryza sativa) is usually thought of as being highly tolerant of flooded conditions. Not only is it able to germinate without oxygen, but green leaves and stems are capable of a powerful, ethylene‐mediated elongation response (Vriezen et al., 2003) that can quickly return leaves or stems into contact with the air. Deepwater and floating ecotypes are particularly well known for this, although the trait is expressed to some extent in most if not all ecotypes of O. sativa. However, for small seedlings, temporary flooding in lowland rice‐growing regions of Asia is often too deep for the elongation escape mechanism to be effective and the plants suffer serious injury or are killed. Causes of this injury and ways to improve tolerance have been the subject of a 4·5‐year project (‘Rice for Life’) funded by the European Commission under its INCO‐DC programme. Work arising from this project is included in this Special Issue. It has benefited substantially from the use of submergence‐resistance lines derived from a primitive Indian farmer variety, and much is now known about the mechanisms of injury and tolerance (Jackson and Ram, 2003). Work on the levels of fermentative enzymes (Mohanty and Ong, 2003) and on volatile emissions using laser photoacoustics (Boamfa et al., 2003) have largely discounted oxygen shortage as necessarily the principal cause of submergence injury in rice. Instead, lack of photosynthetic fixation and enhanced leaf senescence coupled with increased metabolic demands by fast underwater elongation seem largely to be responsible. Molecular genetics has pinpointed a region on chromosome 9 that is closely associated with tolerance, slow underwater elongation, retarded senescence (Toojinda et al., 2003) and ethylene insensitivity. DNA markers, fine mapped to this locus, have proved to be inextricably linked with the inheritance of the tolerance trait. A breeding programme has successfully produced a submergence‐tolerant variety of a Thai fragrant rice that possesses the agronomic and culinary characteristics needed for commercial success and carries a molecular marker closely associated with the tolerance trait (Siangliw et al., 2003). This demonstrates that marker‐assisted breeding for submergence tolerance in rice is now a practical possibility. It also opens the way towards identifying the gene(s) responsible by means of chromosome walking and related techniques.

This Special Issue brings together work from most of the leading laboratories studying plant responses and adaptation to impeded aeration. The progress it documents since the last Annals of Botany Special Issue on this subject (1997) sees a greater emphasis on molecular genetics and the adoption of its techniques by ecophysiologists, physiolog ists and plant breeders, as well as cell biologists. It mirrors the welcome breakdown of barriers that once differentiated the various disciplines within the plant sciences now that an increasingly shared terminology and set of methods allow information to move more easily between scientists with diverse research targets. Clearly, research into stress caused by poor aeration is a rapidly developing into a cross‐disciplinary science. We trust that this Special Issue faithfully reflects this and will help to promote further substantial advances in the future.

References

Author notes

1Department of Plant Ecology, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands, 2Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands, 3Timiriazev Institute of Plant Physiology RAS, 35 Botanicheskaya, 127276 Moscow, Russia and 4School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK