5. THE ROLE OF TEMPERATURE IN seed germination
Dormancy is one of the most important factors inhibiting seed
germination and hindering productivity of field crops (Bentsink &
Koornneef, 2008; Yildiz et al., 2017). Survival of a dormant seed is
ensured by showing apparent metabolic arrest, enduring unfavorable
environmental conditions and timing germination for the correct season
(Bentsink & Koornneef, 2008; Bewley, 1997; Roberts, 1972a). Even at a
dormant state, seeds continuously deteriorate and are still susceptible
to a wide range of environmental fluctuations, such as temperature,
moisture content and oxygen pressure, lately influencing seed viability
(Ellis & Roberts, 1980a, 1980b; Owen & Ashton, 1956; Roberts, 1972b).
Specifically, seed exposure to warm temperatures for a long period of
time may act as catalyzer for dehydration (Berjak & Pammenter, 2013;
Silva, 1998; Syeda, Khan, & Mohmand, 2000). For instance, rice and
wheat seeds exposed to warm temperatures, 40°C for 40 days and 37-50°C
for 12 months, respectively, show decreased longevity when compared to
the control (Ellis, Hong, & Jackson, 1993; Nasreen, 1999).
The capacity to trigger seed germination at the right time is a key
aspect in crop management and this is correlated with the level of seed
dormancy (Benech-Arnold, Rodriguez, & Batlla, 2013). Deeply dormant
seeds result in delayed germination or no germination at all even under
favorable conditions, in contrast, a shallow dormant seed might exhibit
pre-germination or even germinate while still attached to the mother
plant, known as preharvest sprouting (Rodríguez, Barrero, Corbineau,
Gubler, & Benech-Arnold, 2015; Soppe & Bentsink, 2016)(Fang & Chu,
2008; S. Liu et al., 2015). Breaking dormancy and coordinating
germination is also critical during malt production, in which barley
seeds undergo germination triggering processes (K. Shu et al., 2015;
Ullrich, Han, & Jones, 1997). Although preharvest sprouting is highly
species and genotype-dependent, it is mostly observed after exposing
plants to a rainfall or high moisture air conditions, but also occurs
upon exposing the plants to high temperatures during the grain
ontogenesis stage (Figure 4E ). During grain ontogenesis, low
temperatures produce higher level of seed dormancy and better
physiological mature seeds than control temperatures (Nyachiro, Clarke,
DePauw, Knox, & Armstrong, 2002).
Among the genes extensively studied by having a role in germination, two
of the most important players have their expression level regulated by
temperature: MOTHER OF FT AND TFL1 (MFT ) and DELAY
OF GERMINATION 1 (DOG1 ) (Bentsink, Jowett, Hanhart, &
Koornneef, 2006; Xi, Liu, Hou, & Yu, 2010). MFT is suggested to
be the causal gene for the wheat seed dormancy QTL varying across a
temperature range (Nakamura et al., 2011). Grains from plants at
seed-setting stage that were exposed to high temperatures regimes (25°C)
show an abnormally low expression of MFT . In contrast, wheat
grains matured under lower temperature (13°C) show an increased
transcript level of MFT . In rice, OsMFT2 knock-out lines
showed preharvest sprouting under high temperature and rainy weather,
whereas wild type plants and overexpression lines did not (Song et al.,
2020). In parallel, DOG1 transcript levels fluctuate according to
both dormancy level and soil temperature in buried seeds, with low
temperatures showing a higher level of DOG1 than high
temperatures (Footitt, Douterelo-Soler, Clay, & Finch-Savage, 2011;
Graeber et al., 2014; Nakabayashi et al., 2012). DOG1 is
suggested to play a role in balancing ABA and GA levels by promoting ABA
biosynthesis and GA catabolism, hormones known for promoting and
breaking dormancy, respectively (P. Li, Ni, Ying, Wei, & hu, 2019; A.
Yan & Chen, 2017).
In short, dormancy level and establishment during the seed maturing
stages are tightly correlated to the temperature plants or seeds are
exposed to. Generally, lower temperatures result in increased dormancy
depth; in contrast, plants or seeds exposed to supra-optimum temperature
regimes show shallow dormancy, and therefore may drive occurrence of
undesirable events such as preharvest sprouting. For crops, the
domestication process already resulted in selection of less dormant
cultivars than the ones found in the nature (Benech-Arnold et al.,
2013); however, with the warming trend observed and predicted for
climate changes, seed dormancy level might decrease even more, leading
to more common productivity losses and decrease in grain quality.
After dormancy is broken by exposing the seed to specific conditions,
environmental factors, such as temperature, trigger physiological and
biochemical processes causing the seed to germinate. Although
temperature positively correlates with accelerated germination for
multiple species (Barpete et al., 2015; Buriro et al., 2011), once the
species-optimum temperature is reached, every increase from that point
decreases germination rate rapidly (Lamichhane et al., 2019; Tyagi &
Tripathi, 1983).
7. BIOCHEMICAL PROCESSES
UNDER HIGH TEMPERATURE
High temperature affects several biochemical processes in plants. High
day temperature impacts photosynthesis (light-dependent reactions and
carbon assimilation) and photorespiration (Ahammed, Xu, Liu, & Chen,
2018; Ainsworth & Ort, 2010; Bianchetti et al., 2020; Crafts-Brandner
& Salvucci, 2002; Gupta et al., 2013; Kume, Akitsu, & Nasahara, 2019;
Lipova, Krchnak, Komenda, & Ilik, 2010; Nagar et al., 2015; Sharma,
Andersen, Ottosen, & Rosenqvist, 2015), while respiration is mainly
affected by high night temperature (Dusenge et al., 2019)(Figure 5) .
Rubisco activase (Rca) regulates the proportion of catalytically active
Rubisco, the central photosynthetic enzyme (Bracher, Whitney, Hartl, &
Hayer-Hartl, 2017; Portis Jr, 2003) (Figure 5) . Noteworthy, a
functional Rca gene encodes two or more isoforms based on
alternative splicing of pre-mRNA in a temperature-dependent manner. One
of the isoforms is more thermotolerant in crops (Crafts-Brandner &
Salvucci, 2002; Scafaro et al., 2018; Scafaro, Bautsoens, den Boer, Van
Rie, & Galle, 2019; Yamori, Masumoto, Fukayama, & Makino, 2012; Yin et
al., 2014).
Notably, efficient photosynthesis depends on how the Rubisco enzyme
(carboxylase or oxygenase) discriminates between CO2 and
O2 as the substrate (Figure 5) .
Photorespiration, a major productivity limitation for C3 crops, is
exacerbated as temperature increases. A decreased
[CO2]/[O2] ratio due to the
reduction of stomatal conductance caused by warm temperature, results in
the decreased Rubisco specificity for CO2 relative to
O2 (Walker, VanLoocke, Bernacchi, & Ort, 2016).
Compared with Rubisco, the rate of regeneration of the
CO2 acceptor ribulose 1,5-bisphosphate (RuBP) is more
sensitive to higher temperature (e.g. less ATP supply caused by the
impaired electron transport) (Sage, 2002). In maize, however, Rca and
Rubisco activation are the major limitation to net photosynthesis
(Crafts-Brandner & Salvucci, 2002).
In addition, mean night-time temperatures are rising at a faster rate
than those during the daytime (Davy, Esau, Chernokulsky, Outten, &
Zilitinkevich, 2017; Sadok & Jagadish, 2020), which speeds up
respiration and results in crop yield and quality reduction (Coast,
Šebela, Quiñones, & Jagadish, 2020; Dusenge et al., 2019; Impa et al.,
2019; Impa et al., 2020; Schaarschmidt et al., 2020).
Acclimation of the above photosynthetic reactions to heat stress is
significant when the temperature is elevated gradually, which, however,
is less likely during sudden heat waves or intense heat stress (Posch et
al., 2019; Way & Yamori, 2014). These plastic adjustments can allow
plants to photosynthesize more efficiently at their new growth
temperatures (Kaur, Sinha, & Bhunia, 2019; Ruiz-Vera, Siebers, Drag,
Ort, & Bernacchi, 2015).