Vol.:(0123456789) 1 3
Acta Physiologiae Plantarum (2020) 42:117
https://doi.org/10.1007/s11738-020-03107-y
ORIGINAL ARTICLE
Nitrate‑mediated maintenance of photosynthetic process
by modulating hypoxic metabolism of common bean plants
Douglas Antônio Posso
1
· Junior Borella
1
· Gabriela Niemeyer Reissig
1
· Luciano do Amarante
1
·
Marcos Antonio Bacarin
1
Received: 24 August 2019 / Revised: 2 June 2020 / Accepted: 10 June 2020
© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2020
Abstract
Nitrate has been reported to improve tolerance of plants under fooding by modulating carbon and nitrogen metabolism of
root cells; however, the extent to which nitrate modulates the photosynthetic process is not well understood. This work aimed
to evaluate the photosynthetic process by nitrate-mediated modulation of hypoxic metabolism in the root of common bean
plants (Phaseolus vulgaris L.) under fooding and recovery conditions. Three groups of common beans [N
2
-fxing (N
2
)],
N
2
-fxing pre-hypoxic nitrate-treated (N
2
+ NO
3
−
), and nitrate (NO
3
−
)-supplied plants] were grown in vermiculite and the
root system was subjected to fooding for 48 h at the early reproductive stage. After fooding, plants returned to normoxic
conditions per 24 and 72 h for recovery. Plants from N
2
+ NO
3
−
and mainly NO
3
−
groups maintained transpiration rate (E)
and CO
2
assimilation under root-fooding, which was not shown by N
2
-fxing plants. No changes in the dynamic dissipation
of photosynthetic energy were evidenced in leaves of NO
3
−
plants upon fooding, besides an increase in nitrate reductase (NR)
activity and a decrease in fermentative enzymes in roots. Reactive oxygen species (ROS) and antioxidative enzymes increased
in leaves and decreased in roots. Nitrate-mediated maintenance of the photosynthetic process may be related to induction in
NR activity in roots to alleviate the toxic efects of fermentation through a decrease of fermentative enzyme activity.
Keywords Antioxidant system · Fermentative enzymes · Flooding · Nitrate reductase · Nitrogen · Photosynthesis
Introduction
Common bean (Phaseolus vulgaris L.) is an important food
in Brazil and can provide up to 30% of protein for human
consumption. However, about 28 million hectares are food-
prone located in the lowlands of Cerrado and in the South
of Brazil (Jackson and Colmer 2005). Flooded areas are
increasing worldwide due to climate changes (Bailey-Serres
et al. 2012; Limami et al. 2014) which reduces food pro-
duction (USDA 2015). Such areas can be used to increase
food production in a crop rotation with the current rice crop-
ping system, besides that, the use of legume plants in a crop
rotation can improve soil conditions especially by providing
nitrogen, break pests and diseases and contributing to reduc-
ing weed cycles (Garcia et al. 2020).
Legumes, such as common bean (Phaseolus vulgaris L.),
are sensitive to fooding conditions (Loureiro et al. 1998;
Amarante et al. 2006; Sánchez et al. 2011; Justino and Sodek
2013; Borella et al. 2017; Posso et al. 2018). Flooded soils
limit the oxygen difusion in water which is 10
4
times slower
than in air (Armstrong et al. 1994). Flooding impairs oxygen
supply to the roots and nodules, shifting aerobic to anaero-
bic respiration (Limami et al. 2014). Hypoxia increases the
"Pasteur efect" in root cells by speeding up glycolytic reac-
tions to provide energy supply due to inhibition in oxidative
phosphorylation (Summers et al. 2000). To keep glycolysis
running in root cells under fooding, the fermentative path-
way is rapidly activated to continuously regenerate NAD
+
and maintain low ATP production at level substrate (van
Dongen and Licausi 2015).
Several studies have reported that exogenous nitrate
supplementation to plants increases the redox state in root
tissues upon hypoxia conditions (Stoimenova et al. 2003;
Oliveira et al. 2013b; van Dongen and Licausi 2015). The
Communicated by S. Esposito.
* Junior Borella
borellaj@gmail.com
1
Department of Botany, Federal University of Pelotas, C.P.
354, Pelotas, RS 96160-000, Brazil