1. Introduction
Crop waterlogging is increasingly a global problem due to increased frequencies of extreme climate events (Wollenweber, Porter, & Schellberg, 2003). Globally, excessive water and poor soil drainage constraints adversely affect ~10% of arable land area (Setter & Waters, 2003), with average annual economic losses caused by crop waterlogging amounting to tens of billions of US dollars from 2004 to 2013 (Hirabayashi et al., 2013). With climate change, more than 10% of agricultural regions will have greater risk of waterlogging due to higher frequencies and greater magnitudes of extreme rainfall events (Chang-Fung-Martel, Harrison, Rawnsley, Smith, & Meinke, 2017; Hirabayashi et al., 2013).
Waterlogging is a ‘wicked problem’ in that it is highly complex and multi-faceted. In field crop experimental trials, waterlogging driven by excessive rainfall or subsurface or lateral flooding may have poor reproducibility, because waterlogging-prone environments have considerable complexity, including variable dimensions of time, space, biology and chemistry. Thus, methods with which such events are analysed and quantified in a farming systems context requires careful consideration (Harrison, Cullen, & Armstrong, 2017; Harrison, Cullen, & Rawnsley, 2016).
Barley crops (Hordeum vulgare L. ) are currently cultivated in more than 100 countries for use as animal feed and human consumption (Zhou, 2009). Global barley production has diminished over the last two past decades, decreasing from 155 Mt tons in 2008-9 to 142 Mt in 2017-18 (Statista, 2020). Part of this decline is due to increased frequency of waterlogging and susceptibility of barley to waterlogging stress damage (Setter & Waters, 2003). In many contexts, improving crop tolerance to minor waterlogging is generally cost effective, however under severe waterlogging, combined agronomic, engineering and genetic solutions are more effective (Manik et al., 2019).
Defined physiologically, waterlogging tolerance is the survival or maintenance of growth under waterlogging relative to non-waterlogged conditions (Gibbs & Greenway, 2003; van der Moezel, Pearce-Pinto, & Bell, 1991). Oxygen deficiency in soil pores caused by waterlogging reduces root growth, leading to premature leaf senescence and tillering, inhibition of dry matter accumulation and production of sterile florets. In combination, such effects stun kernel number and weight, ultimately penalising potential grain yield (de San Celedonio, Abeledo, Brihet, & Miralles, 2016; de San Celedonio, Abeledo, & Miralles, 2014, 2018; Masoni, Pampana, & Arduini, 2016).
Defined agronomically, waterlogging tolerance is less grain loss relative to susceptible control genotype (Setter & Waters, 2003). Past studies have measured yield declines of 40–79% in waterlogged barley, depending on genotype, growth stage, soil type and duration of waterlogging (de San Celedonio et al., 2014). Yield loss in barley is also likely to be sensitive to the phenological stage with which waterlogging occurs (de San Celedonio et al., 2014). One of the few reports that examined the relationship between yield loss and phenological stage reported that barley was most susceptible during grain filling, moderately susceptible during tillering and least susceptible during seedling stage (Setter & Waters, 2003). However, there are few reports confirming this observation. It is also likely that post-waterlogging growth recovery is a function of genotype of environmental interactions, analogous to crop recovery following defoliation (Harrison, Evans, Dove, & Moore, 2011a, 2011b).
Waterlogging tolerance is likely to be a complex trait related to many morphological and physiological traits that are under strong environmental influence (Zhou, Li, & Mendham, 2007). Lack of oxygen causes roots to shift energy metabolism from an aerobic to anaerobic mode, resulting in cellular energy crises (Gibbs & Greenway, 2003). Apart from tolerance to secondary metabolic compounds associated with anaerobic soil conditions (Huang et al., 2015; Pang et al., 2007), tolerant genotypes of barley may adapt to transient waterlogging via development of morphological mechanisms allowing plants to cope with the stress (Herzog, Striker, Colmer, & Pedersen, 2016; Hossain, Araki, & Takahashi, 2011; Kreuzwieser & Rennenberg, 2014). Morphological adaptations include development of adventitious roots with well-formed aerenchyma (Pang, Zhou, Mendham, & Shabala, 2004; Zhang et al., 2015). An aerenchyma is a continuous gas filled channel that occurs under flooded or hypoxic conditions. This enhances internal diffusion of atmospheric and photosynthetic oxygen from the aerial parts to the flooded roots, allowing roots to maintain aerobic respiration (Armstrong, 1979). Waterlogging tolerant barley genotypes such as the wild barley TAM407227 show not only higher adventitious root porosity than sensitive barley genotypes (e.g. Franklin, Naso Nijo), but also have faster development of aerenchyma (Zhang et al., 2015) under waterlogging conditions. Metabolically, tolerance mechanisms in barley include enhanced activities of glycolytic and fermentative enzymes that increase availability of soluble sugars, and involvement of antioxidant defence mechanisms (e.g. superoxide radicals, hydroxyl radicals and hydrogen peroxide) against post-stress oxidative damages under anaerobic conditions (Armstrong, Brandle, & Jackson, 1994; Davies, 1980; Drew, 1997; Mittler, Vanderauwera, Gollery, & Van Breusegem, 2004; Pan et al., 2019; Setter et al., 1997). Contemporary crop breeders are targeting genetic tolerance mechanisms including aerenchyma formation using molecular marker assisted selection. In barley, a major QTL for AF under waterlogging conditions was identified from several waterlogging tolerance genotypes (Broughton et al., 2015; Zhang et al., 2017; Zhang et al., 2016). This QTL was located in the same position as a QTL for waterlogging tolerance on chromosome 4H (Li, Vaillancourt, Mendham, & Zhou, 2008; Zhang et al., 2017; Zhou, 2010; Zhou, Johnson, Zhou, Li, & Lance, 2012). However, allelic differences exist in different parents, with the contribution of AF to field waterlogging tolerance ranging from around 5% to over 80%. A prospective allele from a wild barley identified in past work (Zhang et al., 2016) has been introgressed to a commercial variety, Macquarie, and this new line, Macquarie+, will be used in this study.
In this study, we imposed four waterlogging treatments on six barley genotypes differing in waterlogging tolerance; two genotypes (Macquarie+ and TAMF169) had the allele for AF under waterlogging stress from the wild barley. The objectives of this study were to examine (1) the impact of timing and period of waterlogging on grain yield and yield components, and (2) the contribution of the QTL for AF under waterlogging stress to mitigate yield loss.