1 ǀ Introduction
Iron toxicity is a set of severely yield-limiting disorders associated
with high concentrations of reduced ferrous iron (Fe(II)) in submerged
lowland rice soils (Becker & Asch; 2005; Sahrawat, 2005). It is
exclusively a problem of submerged soils, because the low redox
potential associated with exclusion of O2 from the soil
leads to prevalence of reduced, soluble Fe(II), whereas in well-aerated
soils, the dominant form is insoluble ferric Fe(III). It is particularly
a problem on highly-weathered, nutrient-depleted soils rich in Fe
oxides. These typify much of the current and potential rice area in
sub-Saharan Africa, in contrast to the young, fertile, alluvial soils of
the Asian lowlands, where most rice research has been done. Hence iron
toxicity has not been a priority in much of the international rice
breeding effort. However, it is a major constraint to rice in
sub-Saharan Africa. Estimates of the rice area in sub-Saharan Africa
affected by Fe toxicity vary from 20 to 60%, and estimated yield losses
vary from 10 to 90% (Rodenburg et al., 2014; Sikirou et al., 2015).
Ironically, most of the global hotspots of Fe toxicity in rice overlap
with areas where Fe deficiency in human diets is acute, suggesting that
currently-grown rice varieties are not effective in translocating
excessively-available Fe from the soil into the grain (Frei et al.,
2016).
There is large variation in tolerance of Fe toxicity in the rice
germplasm, especially in the O. glaberrima species indigenous to
West Africa (Sikirou et al., 2015), and in sub-species of O.
sativa indigenous to Madagascar (Rakotoson et al., 2019). Modern
high-yielding varieties are far more susceptible than locally-adapted
but low-yielding traditional varieties. If tolerance traits in the
indigenous African germplasm could be incorporated into improved
varieties, this could have a huge impact on African rice productivity
and the sustainable expansion of rice-based farming into new areas, and
hence on overall African food security. However progress with breeding
has been slow. Constraints include the complexity of the phenomenon,
poor understanding of tolerance mechanisms, and a lack of reliable
genetic markers for marker-assisted selection. The importance of
particular mechanisms varies with the type of Fe toxicity, and there are
multiple types and interactions with nutrient deficiencies.
Three distinct types of Fe toxic soil are recognised (Becker & Asch;
2005; Sahrawat, 2005):
- acid sulphate soils in coastal plains and river deltas, in which there
is also extreme acidity and Al toxicity;
- clayey organic soils in swampy highland areas, in which the toxicity
becomes acute later in the season as strongly reducing conditions
develop, and so it tends to be less destructive; and
- poor sandy to coarse-loamy soils in inland valleys, where there is
upwelling of interflow water from adjacent highlands with
highly-weathered soils, and the toxicity lasts throughout the growing
season.
As a result of sensitivity to the local hydrology, there is often large
field-scale heterogeneity in toxicity and dependence on inter-annual
variability in rainfall. Further, there are often also deficiencies of
mineral nutrients, particularly P, K, Ca and Mg (Figure 1). These both
compound the Fe toxicity and are exacerbated by it. Hence symptoms occur
at widely differing Fe concentrations in the plant, associated with
different soil types and landscape positions, and interactions with
hydrology and nutrient levels.
Germplasm screening is complicated by large genotype by environment
effects linked to these multiple interactions. Plant adaptations to the
stress depend on complex below-ground plant-soil interactions. Hence
yield losses are only weakly correlated with above-ground symptoms,
though these are widely used for screening (Sikirou et al 2015). Most
work on tolerance mechanisms has been done in hydroponics, far removed
from field reality, and there has been limited progress with the
genetics of tolerance and gene mapping (Dufey et al., 2015; Matthus et
al., 2015; Melandri et al., 2021; Pawar et al., 2021; Sikirou et al.,
2018). There is a need for an integrated approach to understand the
mechanisms and genetics of Fe toxicity tolerance, taking account of the
complex below-ground plant-soil interactions. In this review, we focus
on these below-ground processes, and interactions between genotype
adaptations and mineral nutrient deficiencies. Above-ground tolerance
mechanisms have recently been reviewed by Aung & Masuda (2020) and Wu,
Ueda, Lai & Frei (2017).