Waterproofing Crops: Effective Flooding Survival Strategies

Extremes in water availability (droughts and floods) have increased in frequency and intensity over the past 50 years in farming regions throughout the world. In the United States, losses in crop production due to flooding were second to drought in many of the past 12 years, with these two abiotic stresses accounting for more than 70% of the reduction in harvests in 2011 (Fig. 1A). That year, insurance payouts due to floods exceeded $3 billion (Fig. 1B), with more than $1.6 billion in losses of maize (Zea mays) and soybean (Glycine max) in Midwestern fields. Over the same time period, flooding caused considerable crop loss in other parts of the world. For example, increased summer rainfall intensity in Europe caused numerous flooding and water stagnation events of economic consequence (Olesen et al., 2011), and floods in Australia impacted both production and prices of wheat (Triticum spp.). Exceptionally severe flooding in Pakistan inflicted $4.45 billion in damage to the wheat, cotton (Gossypium hirsutum), and rice (Oryza sativa) crops in 2010 (Arshad and Shafi, 2010). One of the most flooding-threatened crops is rice. At present, over 35% of the world’s rice acreage is flood prone, and much is in regions of Asia and Africa characterized as food insecure. Financial losses in crop production due to environmental stresses in the United States from 2000 to 2011. Yearly totals are in billions of U.S. dollars in loss of food, fiber, and fuel crops. Data are based on insurance indemnities paid to farmers. Values were determined from the U.S. Department of Agriculture Risk Management Agency Cause of Loss Historical Data. A, Percentage of total crop loss per environmental stress. Percentage losses are the quotient of the amount in billions of U.S. dollars of crop loss to each peril divided by the total crop loss for that given year. Drought, Water deficit stress; Flood, excess moisture, precipitation, or rain; Other, anthropogenic and biotic factors such as fire, insects, and plant disease; Extreme, cyclones, hail, hurricanes, and tropical depression events; Cold, cold weather, including frosts and freezes; Heat, excessive radiant heat and hot winds. B, Total crop losses and the proportion of total loss due to floods in billions of U.S. dollars. A major international goal is to increase overall crop production to meet the anticipated needs of the world’s growing population. To achieve this goal, it is essential to develop and adopt germplasm that is better able to endure abiotic assaults. An example of this is the development of rice varieties that survive transient submergence and their noncommercial dissemination to farmers cultivating flood-prone paddies. In this case, robust submergence tolerance was transferred by marker-assisted breeding from a farmer’s landrace to modern varieties, through the initiatives of the International Rice Research Institute. A detailed understanding of the developmental, morphological, physiological, and molecular mechanisms that underlie flooding tolerance should enable the translation of flooding survival strategies to additional crops to stabilize yields of food, feed, fiber, and fuel. The purpose of this Update is to provide a current overview of plant flooding survival strategies from the organismal to the molecular level, with a focus on crop improvement. Here, the term “flooding” is used to describe the inundation by water of all or part of a plant. We use “waterlogging” to describe flooding of the root system and “submergence” to describe the situation when most or all aerial tissue is under water. Floodwaters can be fresh, stagnant, or saline and affect a plant once or multiple times in a growing season. These inundation events can result from flash floods, seasonal rises in surface water at low elevations, or tidal surges. The sudden saturation of well-drained soil causes rhizosphere microbes to rapidly consume available oxygen, triggering changes in the soil ecosystem that can alter the fixation of nitrogen and the availability of other nutrients to the plant. Floods are often accompanied by a decrease in soil pH, which increases the solubility of toxic metals, including iron and manganese, as well as phosphorus and other elements (Setter et al., 2009; Michalcová et al., 2011). Importantly, the approximately 104-fold reduction in diffusion of gases in floodwaters limits the availability of oxygen and carbon dioxide for aerobic respiration and photosynthesis, respectively. If the water surrounding submerged aerial organs is turbid, light availability for photosynthesis is rapidly diminished. Therefore, flooded organs often must increase catabolic processes to meet ATP demands due to the inefficiency of anaerobic ATP production. Over time, the hydrological signature of natural environments has fashioned plants to enable their habitation of environments with seasonal extremes in water availability (Fig. 2). For example, trees of the Amazon and other tropical floodplains endure several months of partial to complete submergence followed by months of moderate to severe water deficit (Parolin et al., 2010). Annual and perennial species native to riparian flood zones are adapted to flooding events of varying amplitude and duration. The species of these habitats have evolved mechanisms of “tolerance,” enabling the plant to withstand the stress, or “avoidance,” enabling the plant to circumvent the stress (Voesenek et al., 2006; Bailey-Serres and Voesenek, 2008; Colmer and Voesenek, 2009; Bailey-Serres et al., 2012). The two survival tactics that have emerged from physiological and molecular studies are (1) the low-oxygen quiescence strategy, characterized by a general restriction in cellular metabolism and growth, displayed by species that regularly endure deep floods of short duration, and (2) the low-oxygen escape strategy, characterized by rapid elongation of underwater stems or leaves to enable photosynthetic tissue to outgrow shallow floodwaters. Although antithetical, both strategies involve ethylene-mediated signal transduction. Plants that inhabit wetlands may also display adaptive features that facilitate the exchange of gases between aerial and flooded organs, including the ethylene-driven formation of constitutive or induced aerenchyma and adventitious roots as well as thinning of the leaf cuticle and reorientation of chloroplasts to optimize gas exchange. Additionally, leaves may have a sufficiently hydrophobic cuticle to maintain a surface layer of gas that sustains the rapid diffusion of oxygen and carbon dioxide to allow continued stomatal activity, benefiting underwater photosynthesis and respiration (Pedersen et al., 2009; Colmer et al., 2011; Winkel et al., 2011). Examples of survival traits displayed in flooded plants. Elongation growth response: deepwater (left) and lowland (right) rice cultivars after 7 d of partial submergence showing distinctions in internode elongation (Hattori et al., 2009); Arabidopsis (Columbia-0 ecotype) after 3 d of complete submergence in darkness showing petiole elongation (Mustroph et al., 2010); and 6-week-old R. palustris plants grown in air (left) or submerged for 14 d (right) showing petiole elongation (Colmer and Voesenek, 2009). Root aeration: adventitious root formation at the third internode in deepwater rice without (left) and with (right) ethephon treatment (Mergemann and Sauter, 2000); and increased lysigenous aerenchyma after 14 d of stagnant waterlogging (Abiko et al., 2012). Radial oxygen loss barriers formed after 14 d of stagnant waterlogging include suberin deposition in cell walls of hypodermal/exodermal layers and lignin deposition on outer epidermis. Z. nicaraguensis root images are 60 mm from the tip of an adventitious root. Leaf gas films cling to the surface of leaves of many semiaquatic species (Winkel et al., 2011). Unlike aquatic and wetland species, most crops are susceptible to flooding events of short duration, resulting in reductions in growth and yield (Table I). A notable exception is lowland rice, which is typically transplanted as a cluster of seedlings to or to 50 deep that are by or precipitation, respectively. are shallow paddies. The to with a flooded root system is by the constitutive development of aerenchyma and barriers that oxygen loss by diffusion and the of (Colmer and Voesenek, 2009). rice by farmers is of more For example, the of of can escape a seasonal flood by underwater elongation of the These or rice varieties are of complete submergence maintain photosynthetic tissue in air to fuel growth and are submergence with the to survive due to flash floods in for more than et al., 2010). are also that can be shallow than that can oxygen availability et al., et al., 2012). 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