Applying Genomics Tools for Breeding Submergence Tolerance in Rice - Translational Genomics for Crop Breeding: Abiotic Stress, Yield and Quality - page 19

intolerant plants, leads to leaf elongation growth
in the attempt to grow to the water surface, that
is, toward the light and oxygen (Figure 2.3c).
In contrast, plants with the tolerant SUB1 locus
and transgenics that overexpress SUB1A-1 (Xu
et al. 2006) enter into a “quiescent” state that pre-
serves carbohydrate reserves and limits anaer-
obic metabolism (Fukao et al. 2006; Barding
et al. 2012). This tolerance strategy limits the
energy crisis caused by carbohydrate starvation
or reduced mitochondrial ATP generation under
flooded, that is, low-oxygen conditions.
Leaf elongation under submergence is trig-
gered by increased synthesis and entrapment of
ethylene (Bailey-Serres and Voesenek 2008) and
a subsequent decrease in abscisic acid (ABA) due
to altered synthesis or enhanced turnover. This
triggers an increase in levels of or sensitivity to
gibberellins (GA) and a GA-dependent growth
response (Figure 2.3d). Comparative analyses
of intolerant and tolerant NILs and transgen-
ics revealed that SUB1A has no effect on the
degradation of ABA but alters GA-dependent
elongation growth under submergence. This
process is regulated by two GA-signaling
repressor proteins, SLENDER RICE-1 (SLR1)
and SLR1 LIKE-1 (SLRL1). In Sub1 rice
and in SUB1A-1 overexpression lines, SLR1 and
SLRL1 transcript and protein accumulation was
higher in submerged tissues, thereby maintain-
ing inhibition of GA-mediated growth responses
(Fukao and Bailey-Serres 2008). Numerous
other genes, including many transcription fac-
tors, are additionally differentially regulated dur-
ing submergence as was shown by a comparative
microarray gene expression analysis (Jung et al.
2010). As a result of the repression of the GA
response, Sub1 plants are significantly shorter
than intolerant plants once floodwaters recede.
Because of the repressed growth and additional
physiological adaptations (Fukao et al. 2006),
tolerant plants retain sufficient energy reserves
for growth following submergence. In contrast,
the elongated and chlorophyll-deficient leaves
of intolerant plants lodge and generally do not
renew growth (Figure 2.3c).

Additionally, upon de-submergence, plants
experience severe oxidative stress because they
are exposed to atmospheric oxygen and natural
(high) light. This leads to the formation of high
concentrations of cell-toxic reactive-oxygen
species (ROS) and cell death. It has been shown
that, in SUB1A-1 genotypes, accumulation of
superoxide and hydrogen peroxide as well as
lipid peroxidation is lower than in intolerant
genotypes (Fukao et al. 2011). In agreement with
this, the authors have shown that abundance of
transcripts encoding ROS-scavenging enzymes
(ascorbate peroxidase, superoxide dismutase,
catalase) is higher in Sub1 genotypes. Further-
more, SUB1A-1 transcript abundance increased
after treatment with methyl viologen (paraquat),
which stimulates ROS production in chloroplasts
(Fukao et al. 2011), suggesting that SUB1A-1 is
directly responsive to ROS. Taken together, the
data suggest that SUB1A protects plants in sub-
merged fields in two ways: (1) inhibition of GA-
induced elongation growth, thereby preventing
exhaustion of carbohydrates and an energy cri-
sis during submergence; and (2) up-regulation
of the ROS-scavenging system, thereby pro-
viding

protection against cell damage upon

de-submergence.
Recently it was demonstrated in Arabidop-
sis that the five ERF genes of the subfamily VII
are substrates of an oxygen-regulated branch of
the N-end rule pathway of targeted proteolysis
(Gibbs et al. 2011). Members of this gene family
in rice include SUB1A as well as the SNORKEL
genes. The N-end rule pathway of targeted pro-
teolysis is important for sensing of low oxy-
gen and it regulates the expression of hypoxia-
responsive genes in Arabidopsis . The substrates
of turnover are constitutively synthesized ERF
genes, including RAP2.12 . Under aerated condi-
tions, RAP2.12 is stabilized by interaction with
the membrane-localized acyl-CoA-binding pro-
tein (ACBP) 1 and 2 (Licausi et al. 2011). Under
low-oxygen conditions, RAP2.12 is released
from the plasma membrane and moves into the
nucleus, where it positively regulates the expres-
sion of hypoxia-responsive genes. Under aerated