1 | INTRODUCTION
As the first cereal crop in the world, maize production is important to
ensure food security (FAO, 2020).
Because of the increasing population and feed demand due to diet shift
in many areas, the continuous improvement of maize yield is a great
challenge in the new era. Maize is sensitive to abiotic stresses such as
drought and heat, which are major environmental factors that limit crop
growth and productivity (Bonfante et al., 2015; Lizaso et al., 2018;
Rossini, Maddonni, & Otegui 2016; Shen et al., 2018; Waha, Müller, &
Rolinski, 2013). Drought and heat stress has been becoming more sever in
time and over space around the world since 1980 (Dai, Trenberth, &
Qian, 2004; Sheffield, Wood, & Roderick, 2012; Wang, Marija, Dong,
Susanne, & Bernd, 2014; Harrison, Tardieu, Dong, Messina, & Hammer,
2014). Heat stress is frequently associated with reduced availability of
water (Lesk, Rowhani, & Ramankutty, 2016; Wang et al., 2018), and the
occurrence of drought accompanied by heat stress is predicted to
increase in future (IPCC, 2014). Therefore, the understanding of
independent and combined drought and heat stress impacts on maize during
the whole growth duration and the
underlying mechanism is pivotal to promote breeding and targeted
management measures.
Across the global maize production area, the combined drought and heat
stress mostly occurred around flowering (Lesk, Rowhani, & Ramankutty,
2016; Wang et al.,
2018).
During this stage, the adverse impacts of the stresses on the male and
female maize organs for the seed-set and seed formation have been
frequently reported (Bassetti and Westgate, 1993; Edreira, Carpici,
Sammarro, & Otegui, 2011; Marceau, Saint-Jean, Loubet, Foueillassar, &
Huber, 2012; Sánchez, Rasmussen, & Porter, 2014; Wang et al., 2018).
The previous studies indicated that maize kernel number was
significantly reduced in the stresses because of low pollen number and
pollen viability, slow silk-growth and ovary-growth rate, and
weak silk receptivity (Alam et al., 2017;
Dresselhaus, & Franklin-Tong, 2013; Wilhelm, Mullen, Keeling, &
Singletary, 1999; Oury, Tardieu, &
Turc, 2016; Oury et al., 2016). For example, the drought stress from
tassel emergence to 6 days after silking decreased the kernel numbers by
42-77% (Oury et al., 2016). The heat stress in 15 days from start of
silking onwards reduced the kernel numbers by 75% (Edreira, Carpici,
Sammarro, & Otegui, 2011). Most of current studies has analyzed the
impacts on maize kernel number by the heat and drought stresses, but the
persistent impact of the stresses around flowering on the subsequent
maize kernel development has received limited attention. Furthermore,
limited information is available on the individual and combined impacts
of heat and drought stress during the early flowering stage on the
qualitative aspects in maize grain weight.
For wheat, some studies indicated that the early (around flowering)
drought and heat stress shortened leaf area duration (Cristina, Daniel,
Calderini, & Gustavo, 2007), decreased chlorophyll index (Hlaváováet
al., 2018) and reduced net photosynthetic rate (Wang, Marija, Dong,
Susanne, & Bernd, 2014). The subsequent impact of early heat stress on
grain weight in field was also observed (Abeledo, Savin, & Slafer,
1999; Calderini, Savin, Abeledo, Reynolds, & Slafer, 2001; Cristina,
Daniel, Calderini, & Gustavo, 2007). For barley, the heat exposed to
booting-anthesis stage decreased grain weight by 13.4% (Cristina,
Daniel, Calderini, & Gustavo, 2007). For rice, grain yield was reduced
by 24% because of the combined drought and heat stress at anthesis
(Amjikarai, Chenniappan, & Dhashnamurthi, 2018). These observations
showed grain development was limited by the source (canopy structure and
function), which was affected by the early stress. Whether the sink
(grain) development was also limited by the early stress around
flowering if source supply was not limited since grain filling remained
unclear. Meanwhile, the underlying physiological mechanism for
the response of subsequent grain
development with both limited and non-limited source supplies to the
early heat stress should be further addressed.
It has been generally accepted that the grain weight was determined
during the period since grains were actually set (Egli, 2004).
Therefore, most studies for grain weight focused on the post-anthesis
stage for grain filling (Royo, Abaza, Blanco, García, & Luis F, 2000).
In this study, we hypothesized that the independent and combined drought
and heat stress around flowering stage still has significant effect on
the subsequent grain filling process even with adequate source supply
although the stress was relieved since the beginning of grain filling.
The purpose of this study was to (i)
detect and compared the impacts of
the drought stress, heat stress, and combined drought and heat stress
around flowering on the subsequent kernel weight, (ii) compare the
response of subsequent grain development to the early stresses with
limited source supply in field and adequate source supply in laboratory
incubation, (iii) investigate the underlying mechanism of the above
responses. This study included three experiments (Figure 1). In
Experiment 1 (Exp. 1), maize plants were subjected to drought stress,
heat stress and combined drought and heat stress during the short period
from tassel emergence to ovaries fertilization in ponds covered with a
rain shelter, and the fertilized ovaries continued to grow in field. In
Experiment 2 (Exp. 2), the fertilized ovaries in Exp. 1 were vitro
cultured in the chamber with favorable growth conditions in laboratory
incubation. Sufficient source supply was provided for kernel growth in
vitro cultured, which was proved to be an useful method for
investigating the grain development (Burle, Gengenbach, Robert, 1994;
Zhang et al., 2017). In Experiment 3 (Exp. 3), maize plants were
subjected to similar stress with Exp. 1 around flowering in pots, the
fertilized ovaries were also vitro cultured for the measurement of
carbohydrate metabolism and starch synthesis in grain. Our study reports
for the first time about the subsequent impacts of independent and
combined drought and heat stress around flowering on maize grain filling
and thus necessities the need for development of maize genotypes
resilient to these stresses, especially to combined stress environments.