The era of cultivating smart rice with high light efficiency and heat tolerance has come of age

Abstract

How to improve the yield of crops has always been the focus of breeding research. Due to the population growth and global climate change, the demand for food has increased sharply, which has brought great challenges to agricultural production. In order to make up for the limitation of global cultivated land area, it is necessary to further improve the output of crops. Photosynthesis is the main source of plant assimilate accumulation, which has a profound impact on the formation of its yield. This review focuses on the cultivation of high light efficiency plants, introduces the main technical means and research progress in improving the photosynthetic efficiency of plants, and discusses the main problems and difficulties faced by the cultivation of high light efficiency plants. At the same time, in view of the frequent occurrence of high-temperature disasters caused by global warming, which seriously threatened plant normal production, we reviewed the response mechanism of plants to heat stress, introduced the methods and strategies of how to cultivate heat tolerant crops, especially rice, and briefly reviewed the progress of heat tolerant research at present. Given big progress in these area, the era of cultivating smart rice with high light efficiency and heat tolerance has come of age.

Full text

The era of cultivating smart rice
with high light efficiency and
heat tolerance has come of age
Qiuping Shen
1,2
†
, Yujun Xie
1,2
†
, Xinzhe Qiu
2
and Jinsheng Yu
1,2
*
1
The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province,
Zhejiang A & F University, Hangzhou, China,
2
College of Advanced Agricultural Sciences, Zhejiang
A & F University, Hangzhou, China
How to improve the yield of crops has always been the focus of breeding
research. Due to the population growth and global climate change, the
demand for food has increased sharply, which has brought great challenges
to agricultural production. In order to make up for the limitation of global
cultivated land area, it is necessary to further improve the output of crops.
Photosynthesis is the main source of plant assimilate accumulation, which has
a profound impact on the formation of its yield. This review focuses on the
cultivation of high light efficiency plants, introduces the main technical means
and research progress in improving the photosynthetic efficiency of plants, and
discusses the main problems and difficulties faced by the cultivation of high
light efficiency plants. At the same time, in view of the frequent occurrence of
high-temperature disasters caused by global warming, which seriously
threatened plant normal production, we reviewed the response mechanism
of plants to heat stress, introduced the methods and strategies of how to
cultivate heat tolerant crops, especially rice, and briefly reviewed the progress
of heat tolerant research at present. Given big progress in these area, the era of
cultivating smart rice with high light efficiency and heat tolerance has come
of age.
KEYWORDS
smart rice, high light efficiency, C4 engineering, heat tolerance, breeding
Introduction
Due to the limited arable land worldwide, human beings have been committed to
continuously improving the output of crops. Most of the yield accumulation of plants
comes from the assimilation products of photosynthesis. The photosynthetic yield of any
crop depends on the effective solar radiation, radiation capture efficiency and
photosynthetic efficiency throughout the growing season (Jansson et al., 2018).
Because of the continuous growth of the world’s population, it is expected that the
global population will reach 9 billion by 2050, which means that the demand for food will
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Joseph Edwards,
University of Texas at Austin,
United States
REVIEWED BY
Prachi Pandey,
National Institute of Plant Genome
Research (NIPGR), India
Guanjun Huang,
Huazhong Agricultural University,
China
*CORRESPONDENCE
Jinsheng Yu
jinshyu@zafu.edu.cn
†
These authors have contributed
equally to this work
SPECIALTY SECTION
This article was submitted to
Plant Systematics and Evolution,
a section of the journal
Frontiers in Plant Science
RECEIVED 17 August 2022
ACCEPTED 16 September 2022
PUBLISHED 07 October 2022
CITATION
Shen Q, Xie Y, Qiu X and Yu J (2022)
The era of cultivating smart rice with
high light efficiency and heat tolerance
has come of age.
Front. Plant Sci. 13:1021203.
doi: 10.3389/fpls.2022.1021203
COPYRIGHT
© 2022 Shen, Xie, Qiu and Yu. This is an
open-access article distributed under
the terms of the Creative Commons
Attribution License (CC BY). The use,
distribution or reproduction in other
forums is permitted, provided the
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permitted which does not comply with
these terms.
TYPE Mini Review
PUBLISHED 07 October 2022
DOI 10.3389/fpls.2022.1021203

rise sharply, bringing great challenges to agricultural production
(Stratonovitch and Semenov, 2015). In order to meet the food
requirement, the existing food production must increase by
nearly 70% (Lobell et al., 2011) and increasing the yield
accumulation of plants by various means will be the most
important way.
High light efficiency refers to higher light utilization
efficiency under low light and low CO
2
concentration, or
stronger photosynthesis than other plants under the same
conditions. Although the current global CO
2
concentration has
increased, which seems beneficial to crop photosynthesis, this
change is concentrated in the past few decades since 1975, and
plants lack sufficient time to adapt to such rapid environmental
changes. In addition, the decline of nitrogen uptake by plants
under high CO
2
concentration and the source-sink limitation
also imply that the method of changing CO
2
concentration to
increase yield is not sustainable (Drake et al., 1997;Long et al.,
2015;Zhu et al., 2021). Theoretically, the potential
photosynthetic efficiencies of C3 and C4 plants were
maximally able to reach 0.046 and 0.060, respectively.
However, the current photosynthetic efficiencies of the two
types of plants during the growing season only reach 47% and
57% of their theoretical values, respectively, and still have a large
rising space (Zhu et al., 2010;Hein et al., 2021). In addition, the
frequent occurrence of extreme high temperature caused by
climate change in recent years has affected the normal
production of a variety of crops, causing plant photosynthesis
to be blocked and production to be reduced. It is estimated that
the yield of rice will decrease by 3%-8% for every 1°C increase in
the average temperature (Paul et al., 2020). This shows that, in
addition to improve the photosynthetic efficiency of plants, it is
also of great significance to ensure that plants can maintain a
normal yield balance under the coming extreme high
temperature. With the advent of post functional genomics in
rice, breeding strategies that utilize beneficial alleles and
eliminate deleterious alleles to optimize crop genome have
broad prospects for designing future crops (Varshney et al.,
2021;Yu et al., 2022), and the era of breeding smart rice with
high light efficiency and heat resistance has come of age.
Research progress of high light
efficiency
Photosynthetic products are synthesized in leaves,
transported to stems and leaf sheaths and stored as NSCs
(non-structural carbohydrates), and then transferred to grains
during grain filling (Hein et al., 2021). There are many factors
affecting plant photosynthesis. Besides the main environmental
conditions such as temperature and light, the morphological
development and genetic regulation of plants are also important
factors limiting their own photosynthesis. The improvement of
photosynthetic rate of crop leaves can be achieved by targeted
control of single component processes, such as improving the
affinity of key enzyme Rubisco (1,5-ribose diphosphate
carboxylation oxygenase) for CO
2
(Long, 1991), increasing leaf
vein density (Feldman et al., 2017), and adjusting stomatal size
and density (Xiong et al., 2022). Furthermore, it is also an
effective way to improve photosynthetic efficiency to explore
key genes affecting photosynthesis through molecular
genetic means.
According to the different carbon fixation products, plants
can be divided into C3 and C4 types. Some important food crops
such as rice and wheat belong to C3 plants, and their
photosynthetic efficiencies largely limited by Rubisco’s
oxygenation activity and photorespiration (Atkinson et al.,
2016;Singer et al., 2019). In contrast, C4 plants can improve
their photosynthetic efficiency by about 30% compared with C3
plants due to their extremely low photorespiration level and CO
2
concentration mechanism (CCM, Langdale, 2011). Studies have
shown that only 10% increase in photosynthetic efficiency can
increase crop yield by nearly 50% (Zhu et al., 2008). It can be
seen that if C4 pathway can be introduced into C3 plants such as
rice, it will make great contributions to improve grain yield.
In addition, with the development of high-throughput
phenotyping technology, people can accurately evaluate the
phenotype of a large number of plants within a short time,
which provides great convenience for breeding (Araus et al.,
2018). In general, the leaves of plants can display different
reflectance values at specific wavelengths due to different
growth conditions. Therefore, the reflection wavelength of
different plant leaves can be obtained by using reflection
spectrum technology, which is very effective for determining
various leaf characteristics including leaf greenness, light
utilization efficiency and leaf pigment content (Tayade et al.,
2022). At the same time, in view of the subtle color change of
leaves caused by chlorophyll decomposition, reflection spectrum
technology is also widely used in determining the senescence
rate of leaves (Hein et al., 2021). This not only provides a rapid
and accurate method for evaluating the photosynthetic efficiency
of different plants, but also provides technical support for
cultivating and screening plants with high photosynthetic
efficiency, so it has great application potential.
Design C4 crops
At present, people have made preliminary exploration in the
design of C4 crops by means of genetic engineering (Ishimaru
et al., 1998;Wang et al., 2012;Lian et al., 2014;Cheng et al., 2016;
Kandoi et al., 2022). Many studies have shown that
overexpression of key photosynthetic enzymes of C4 pathway
helped to improve photosynthetic efficiency of C3 plants.
However, this enhancement effect is not caused by the
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introduction of CCM, but by the increased chlorophyll synthesis
caused by enhanced metabolism (Kandoi et al., 2022). Thus, the
gained effect was quite limited. Given the effect of overexpression
of individual photosynthetic enzymes on the rate of carbon
assimilation, there are several attempts to combinatorically over-
express multiple C4 photosynthetic enzymes to further enhance
photosynthesis. However, the results showed that this approach
not only did not concentrate CO
2
near the chloroplast, but also
produced a slight developmental delay (Häusler et al., 2001;
Taniguchi et al., 2008;Yadav and Mishra, 2020). Since the
current design for C4 crops still stays on single-cell methods
such as overexpression of some photosynthetic genes, this
limited improvement in photosynthetic efficiency can’t bring
substantial improvement in yield (Cui, 2021).
The complex mechanism of C4 pathway is not only reflected
in the types of photosynthetic enzymes. The spatial separation of
C4 plant photosynthesis is the main reason for its formation of
CCM (Furbank, 2017). Mesophyll cells tightly surround Bundle
sheath (BS) cells in the center, making BS cells isolated from
external O
2
and reducing the occurrence of photorespiration.
Moreover, BS cells are significantly larger than C3 plants and
contain more chloroplasts, which greatly improves the
photosynthetic efficiency of C4 plants (Yadav and Mishra, 2020).
On the other hand, the unique Kranz structure of C4 plants’
leaves is another important feature that distinguishes C4 plants
from C3 plants (Figure 1,Lundgren et al., 2014). The leaves of
C4 plants have developed and more BS cells and more dense leaf
vein tissues, and the connection between BS cells and mesophyll
cells is also closer, which promotes the exchange of materials
between them. Compared with C3 plants, C4 plants have higher
material transport efficiency (Wang et al., 2011;Danila et al.,
2016;Cui, 2021). Kranz structure contains many different forms,
but almost all evolved from C3 plants (Sage et al., 2014). Some
genera such as Flaveria and Steinchisma contain both C3 and C4
species or some C3-C4 evolutionary intermediates. Recently,
many more C3-C4 intermediates have been found (Brown et al.,
2005;Marshall et al., 2007;Keerberg et al., 2014;Khoshravesh
et al., 2016). It can be seen that some C3-C4 groups led by
Flaveria are important resources for studying the evolutionary
mechanism of C4 plants, which provides a valuable biological
basis for early attempts to C3 to C4 engineering and for studying
the evolutionary mechanism of Kranz anatomical structure
(Cui, 2021).
Methods of cultivating high light
efficiency plants
Enhancing the carboxylation of Rubisco
Studies have shown that up to 1/2 of Rubisco’s reactions
during photosynthesis are oxygenation reactions (Tcherkez
et al., 2006). Therefore, this enzyme is regarded as one of the
most important targets to improve the photosynthetic efficiency
FIGURE 1
Photosynthetic pathway, leaf structure of C3 and C4 plants and main improvement methods for C3 plants at present. C3 plants on the left and
C4 plants on the right. Blue solid line represents the photosynthetic reaction; blue dotted line represents the transport of substances; black line
represents the catalysis of the enzyme; red dots represent major improvement objectives. RuBP, ribulose-1,5-bisphosphate; Rubisco, RuBP
carboxylase/oxygenase; PGA, 3-phosphoglycerate; PGAld, 3-phosphoglyceraldehyde; GA, glycollic acid; PEP, Phosphoenolpyruvate; PEPC,
Phosphoenolpyruvate carboxylase; OAA, oxaloacetic acid; Mal, malic acid; Pyr, pyruvic acid; NADP-ME, NADP-malic enzyme; PPDK, pyruvate
phosphate dikinase; CCM, carbon concentration mechanism.
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of C3 plants. Some studies suggest that CCM of cyanobacteria
can be introduced into C3 plants (Zarzycki et al., 2013;Hanson
et al., 2016). This special CCM can achieve high CO
2
concentration around Rubisco only through the carboxy
matrix in the cell (Lin et al., 2014). Compared to the general
mechanism by which C4 plants achieve CO
2
enrichment
through spatial separation of photosynthesis, this CCM
mechanism for cyanobacteria is clearly much simpler and thus
very promising for C3 crop improvement. Recently, it has been
found that by introducing five photosynthetic enzymes from Zea
mays into specific cells of rice leaves, the minimum C4 cycle can
be constructed to achieve the purpose of CO
2
concentration and
have little impact on rice. This also provides another strong
evidence for the feasibility of introducing CCM into rice
(Ermakova et al., 2021).
Enhancing the catalytic activity
of Rubisco
In addition, the low catalytic activity of Rubisco is also one of
the main reasonsfor the low photosynthetic efficiency of C3 plants.
Different from the efficient catalytic ability of other enzymes,
Rubisco’s catalytic rate is very slow, and each active site can only
catalyze about 3.7 enzymatic reactions per second, while most other
enzymes can catalyze more than 100 reactions (Parry et al., 2013).
This makes plants need to synthesize Rubisco in large quantities to
compensate for their low catalytic capacity. It is estimated that
plants need to consume up to 50% of leaf soluble protein and 25% of
leaf nitrogen to maintain sufficient photosynthetic rate, which
greatly limits the growth of plants (Lin et al., 2014). Therefore,
improving the catalytic capacity of Rubisco is also an inevitable
problem in cultivating high light efficiency plants.
Bypassing endogenous photorespiration
Photorespiration has become the most important factor
limiting the photosynthetic yield of plants, which can cause 20-
50% yield loss of C3 crops (Wang et al., 2020;Nayak et al., 2022). It
is one of the effective measures to avoid the loss of fixed carbon by
designing and installing the metabolic bypass of photorespiration to
inhibit or bypass the endogenous photorespiration. E. coli can use
glycolate as the sole carbon source and can release CO
2
while
metabolizing (Pellicer et al., 1996). By introducing the glycolic acid
metabolism pathway of E. coli into crops such as Arabidopsis and
potato, the researchers made the plants express some or all glycolic
acid metabolism related genes, reduce or bypass their own
photorespiration, and significantly improve plant photosynthesis
(Kebeish et al., 2007;Nolke et al., 2014). The same method was
applied to the improvement of cucumber, and it was found that the
partial or complete introduction of exogenous glycolic acid
pathway increased the biomass by 44.9% and 59%, respectively
(Chen et al., 2019).
Leaf phenotypic improvement
Besides endogenous genetic regulation, leaf phenotype is
also an important factor affecting photosynthetic efficiency.
More dense leaf veins and smaller and many more stomata
contribute to gas exchange and material transport, which is an
effective method to improve photosynthetic efficiency (Feldman
et al., 2017;Xiong et al., 2022). Furthermore, the size, curl,
inclination angle and other structures of leaves all affect the
photosynthetic efficiency of plants. Through the comparison
between different rice varieties, it was found that the leaves of
rice with high photosynthetic efficiency often have the
anatomical characteristics of larger mesophyll cells, more
chloroplasts, fewer mesophyll cells between adjacent two leaf
veins, and larger chloroplast surface area (Mathan et al., 2021).
The content of chlorophyll and other photosynthetic pigments is
directly related to the photosynthetic potential and primary
productivity. It is generally considered that high chlorophyll
content is an ideal phenotype. However, some studies have
shown that higher chlorophyll may affect the available light of
lower leaves and thus affect the photosynthesis of the whole
plant. Reducing the antenna size to appropriately reduce the
chlorophyll content, on the contrary, contributes to the
improvement of PSII efficiency and nitrogen use efficiency
(Song et al., 2017;Leister, 2022).
Prolonging the photosynthetic period
of leaves
In rice grains, nearly 80% of the reserve substances come
from photosynthesis of leaves after heading (Da Costa et al.,
2022). For example, hybrid maize, because of its longer period of
photosynthetic activity, still maintains a higher chlorophyll
content during senescence relative to normal maize, thereby
increasing grain yield (Wu et al., 2016b). This indicated that it
was a feasible way to achieve high yield by prolonging the
photosynthetic function period of leaves and preventing
premature senescence of leaves. Improving the synthesis
capacity of chlorophyll, slowing down the senescence and
degradation speed of chloroplast, and improving the
antioxidant capacity of chloroplast are the main means to
ensure the photosynthetic efficiency (Khan et al., 2020;Tang
et al., 2020;Yu et al., 2020;Pang et al., 2022). It was found that
leaf senescence may be induced by hexose accumulation. By
applying different concentrations of sucrose to young and
mature leaves, it was found that the electrolyte leakage and
malondialdehyde level of leaves increased under high sucrose
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concentration, resulting in the decrease of leaf photosynthesis
(Asim et al., 2022).
Improve the heat tolerance of plants
In the 21st century, due to the intensification of the
greenhouse effect and global warming, extreme weather occurs
frequently in the world, of which extreme high temperature has
the most serious impact on plants (Zhao et al., 2022). Taking rice
as an example, high temperature will not only affect the normal
synthesis and processing of protein, change the activities of
various enzymes, lead to disorder of energy metabolism and
excessive accumulation of reactive oxygen species, but also cause
poor development of flower organs, affect normal pollination and
fertilization, lead to poor grain development and shortened filling
time, thus reduce the quality and nutritional value of grains (Wu
et al., 2016a;Prasertthai et al., 2022). A series of negative effects
caused serious damage to plant yield (King et al., 2015). It is
estimated that the yield of rice will decrease by 3%-8% for every 1°
C increase in temperature (Paul et al., 2020). With the continuous
change of the global climate, it can be expected that extreme high
temperatures will occur more frequently. Therefore, improving
the heat tolerance of plants to improve the stable yield is one of
the bases to ensure the cultivation of high light efficiency crops.
Plant response to heat stress (HS)
Signal transmission mechanism in plants
Plants need to convert external temperature changes into
internal molecular signals to induce their own heat shock
response (HSR). In higher plants, photoreceptors including
phytochrome and cryptochrome may be the potential
temperature sensors of plants (Miyazaki et al., 2015;Jung
et al., 2016;Legris et al., 2016;Fujii et al., 2017). These
photoreceptors change their activity through temperature
changes, participate in the regulation of various temperature
signaling pathways or directly regulate the temperature sensitive
response of plants Li et al., 2022. In addition, some transcription
factors and regulatory elements also have the characteristics that
their activity changes with temperature, and also have the
potential as temperature sensors. These features include
changes in DNA/chromatin structure, variable splicing of
mRNA, changes in RNA secondary structure, etc., which have
also been reported (Nusinow et al., 2011;Vu et al., 2019;Perrella
et al., 2022). However, most of the temperature receptors
reported and identified at present are to regulate the
morphological change or developmental transition process of
plants under warm-temperature environment, and only one case
of temperature receptors tolerant to extreme high temperature
has been reported (Zhang et al., 2022).
Ca
2+
signaling is considered to be the fastest signal response
in plants (Kan and Lin, 2021). HS affects the fluidity of plasma
membrane and causes a large amount of internal flow of Ca
2+
in
a short time. It can reach the peak in a short period of 15s, thus
rapidly transmitting the external temperature signal (Saidi et al.,
2010). The elevated Ca
2+
level in the cytoplasm induces various
stress responses to tolerant high temperature by activating or
inhibiting the activities of Ca
2+
/CAM related kinases,
phosphatases and transcription factors. In addition, reactive
oxygen species (ROS) have also recently been reported to be
involved in the heat shock response of plants, which activates the
plant’s overall defense mechanism by stimulating stressed tissues
to generate a series of responses while transmitting stress signals
from stressed to non-stressed areas (Zandalinas et al., 2020).
Heat shock protein
When HS occurs, the normal function of the endoplasmic
reticulum is affected, resulting in a large accumulation of
unfolded and misfolded proteins, resulting in cytotoxicity.
Meanwhile, plants will activate the transcription of heat shock
factor (HSF) and induce a large number of heat shock proteins
(HSPs). This kind of special proteins with molecular chaperone
activity can maintain the thermal stability of other proteins and
ensure that other proteins perform correct post-translational
folding. Some HSPs also play a role in the degradation of
abnormal proteins and non-functional proteins (Taipale et al.,
2010;Usman et al., 2017;Kang et al., 2022). HSP is considered to
be one of the most important defense responses of plants under
HS, which can significantly improve the survival rate of plants.
Moreover, many HSPs are not only induced by high temperature
conditions, but also activated by various other stresses such as
hypoxia, drought and heavy metal ions, thus becoming an
important part of plant tolerance under various abiotic stresses.
HS memory
Due to climate change, high temperature usually occurs
temporarily and repeatedly. In order to cope with this
situation, plants have the ability to maintain and acquire heat
tolerance at the end of HS events, so that plants can respond to
repeated HS events more quickly, which is called HS memory
(Charng et al., 2006). HS memory includes two types, namely
type I and type II (Oberkofler et al., 2021). Both types guarantee
that the genes corresponding to them are able to be continuously
induced or show an enhancement of re-induction at the end of
HS. This physiological response is induced by some key HSFs
(such as HSFA2) and involves histone methylation around
memory genes and the maintenance of low nucleosome
occupancy, thus ensuring its efficient induction (Perrella et al.,
2022). HS memory can last up to 5-6 days in Arabidopsis, which
significantly improves the tolerance of plants to high
temperature (Liu et al., 2018).
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Breeding heat tolerant rice by
genetic methods
Directional genetic improvement of rice by molecular
biology has significant advantages over traditional breeding
methods, which can greatly shorten the breeding period and
ensure the accurate improvement of target traits. With the help
of heat-tolerant germplasm resources including N22, various
means were used to explore the molecular mechanism of rice
HSR and identify relevant genes/QTLs, so as to realize the direct
regulation of rice heat response pathway. At present, a large
number of heat resistance related genes have been identified,
which has provided some help for heat resistance breeding of
rice. However, the number of successfully cloned genes is very
limited (Table 1)(Rabara et al., 2021). Therefore, it is still the
focus of rice heat tolerance research to successfully clone the
identified heat tolerance genes and make them be used in
breeding practice.
In recent years, with the development of molecular biology,
some regulatory elements led by E3 ubiquitin ligase and
microRNA have been revealed to participate in the regulation
of heat tolerance in rice and other plants (Ning et al., 2011;Song
et al., 2013;Cui et al., 2017). Different from the genes/QTLs that
directly affect the phenotype of plant traits, these stress response
factors cause the decrease of gene expression or the change of
protein abundance through regulating various metabolic
pathways, and ultimately affect heat tolerance of plants. This
undoubtedly provides a new channel for breeding rice with heat
tolerance. However, although many heat tolerance related
regulatory loci and QTLs have been reported, these studies
cannot further improve rice yield (Khan et al., 2019;Rabara
et al., 2021). In other words, these studies can only guarantee the
stability of rice yield under various high temperature conditions.
Due to the rapid growth of the global population, the current
grain production has been difficult to meet the future demand. It
is difficult to achieve the breeding goal of increasing production
simply by improving heat resistance. A few studies have
identified some genes/QTLs that simultaneously affect rice
heat tolerance and yield, but few of them have been
successfully cloned (Wang et al., 2016b;El-Esawi and Alayafi,
2019;Lo et al., 2020). The ultimate goal of heat-resistant
breeding is to make the rice yield meet the increasing food
demand under future climate conditions. Therefore, it is
necessary to take yield improvement into account when
studying heat resistance.
Improve breeding efficiency
Although the current use of marker-assisted selection (MAS)
to aggregate the main effect QTL or gene of the target trait has
significantly improved the breeding efficiency compared with the
traditional methods, heat tolerance of rice is a complex trait
controlled by multi minor-effect gene loci. Thus, the aggregation
of several major-effect genes alone does not result in a very ideal
phenotype, which limits the further improvement of breeding
efficiency (Spindel et al., 2015).
Genome selection (GS) refers to a method of selection using
high-density molecular genetic markers covering the whole
genome to calculate genome estimated breeding value
(Meuwissen et al., 2001). This method is still a kind of MAS
method in essence, but it has many advantages compared with
general MAS breeding (Varshney et al., 2020). First, GS allows
early selection without detecting for major effect genes affecting
the target trait and frees the reliance of traditional breeding on
phenotypic information with increased accuracy. Moreover, GS
has successfully realized the identification and selection of many
small effect genes, which is more conducive to the improvement
of complex traits (Newell and Jannink, 2014). Finally, compared
with the traditional MAS method, GS is more effective in
improving traits with low heritability and difficult to measure
(Yu et al., 2022). It can be seen that if GS can be applied to
improve heat tolerance of rice, it will reduce or even get rid of the
phenotypic identification, improve the accuracy of selection,
further improve the breeding efficiency, and have a broad
application prospect.
Summary
Photosynthesis, as a direct source of plant yield, has received
extensive attention. Many studies hope to further enhance the
accumulation of plant assimilates by improving photosynthetic
efficiency. The photosynthesis of plants is affected by both itself
and the environment. Due to the limitation of nitrogen
assimilation and source sink, the improvement of plant
photosynthetic efficiency by changing the environmental CO
2
concentration is very limited. It is expected that future research
will still focus on the genetic improvement of plants. The
improvement of photosynthetic pathway or components and
the introduction of C4 pathway are the main research focuses at
present. The former has been reported in a large number, but the
latter is still at an early stage of exploration. In order to realize
plant C3-C4 engineering, the spatial separation of
photosynthesis and Kranz structure are the two key problems
to be solved, and the utilization of some C3-C4 intermediates
point out the promising direction. In addition, with the global
warming and the frequent occurrence of extreme weather, high
temperature has increasingly become one of the important
factors limiting plant yield. HS almost affects all physiological
processes of plants, including photosynthesis, and even causes
plant death in serious cases. Therefore, cultivating heat tolerant
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TABLE 1 The map-based cloned genes related to heat tolerance in rice.
Gene
symbol
MSU Mapping
population
How to clone Coding product Regulation Function donor marker mutation type Reference
OgTT1 LOC_Os03g26970 BC
4
F
2
(6721) Map-based
cloning
a2 subunit of the 26S
proteasome
Positive
regulation
Eliminate cytotoxic
denatured protein
CG14 SSR Point mutation (Li et al., 2015)
TOGR1 LOC_Os03g46610 F
2
Map-based
cloning
DEAD-box RNA helicase Positive
regulation
Regulate rRNA
homeostasis
Zhong Xian
3037
STS, CAPS Single nucleotide G to T
substitution
(Wang et al., 2016a)
OsCAO1 LOC_Os10g41780 cross line
between pale green
leaf mutant and TN1
Map-based
cloning
chlorophyllide an
oxygenase 1
Positive
regulation
impact leaf
senescence
japonica rice
variety
Yunyin
SSR Point mutations lead to
premature termination of
translation
(Yang et al., 2016)
OsBHT LOC_Os01g55270 Cheongcheong/
Nagdong DH line
Map-based
cloning
an Hsps-p23-like calcyclin-
binding protein
Positive
regulation
Participate in HSR
as a molecular
chaperone
CNDH75 SSR Higher expression level (Park et al., 2020)
SLG1 LOC_Os12g39840 F
2
(834 mutants) Map-based
cloning
Cytosolic tRNA 2-
thiolation protein 2
Positive
regulation
Regulate the level of
thiolated tRNA
KY131 whole-
genome
polymorphic
marker
Single-nucleotide substitution
resulting in mis-splicing and the
formation of multiple transcripts
(Xu et al., 2020)
HTS1 LOC_Os04g30760 F
2
(1370 mutants) Map-based
cloning
b-ketoacyl carrier protein
reductase
Positive
regulation
Maintain membrane
stability and
chloroplast integrity
Wuyunjing 7 SSR, STS Single nucleotide substitution (Chen et al., 2021)
PSL50 LOC_Os01g50770 F
2
(170 mutants) Map-based
cloning
A clathrin-associated
adaptor protein complex 1
medium subunit m1
(AP1M1)
Positive
regulation
Negatively regulates
heat-induced
premature leaf
senescence
Zhongjian
100
SSR 1-bp deletion mutation (He et al., 2021)
HES1 LOC_Os08g10600 F
2
Map-based
cloning
UDP-N-acetylglucosamine
pyrophosphorylase
Positive
regulation
play essential roles
in maintaining
chloroplast function
indica rice
(Oryza
sativa) cv
ZF802
SSR Point mutation led to premature
termination
(Xia et al., 2022)
EMF1 LOC_Os01g42520 Ethyl
methanesulfonate
mutagenized
population of Yixiang
1B
Map-based
cloning
A DUF642 protein Positive
regulation
Early flowering YX1B SSR 14‐bp deletion (Xu et al., 2022)
HTH5 LOC_Os05g05740 BC
5
F
2
(7648) Map-based
cloning
Pyridoxal phosphate
homeostasis protein
Positive
regulation
Affect seed setting
rate
HHT3 SSR nucleotide mutation in the
promoter region
(Cao et al., 2022)
OgTT2 LOC_Os03g29370 BC
5
F
2
(7820) Map-based
cloning
AGgsubunit and an
unknown protein
Negative
regulation
Regulate the
biosynthesis of wax
HP21 InDel, CAPS Point mutation led to premature
termination
(Kan et al., 2022)
OgTT3.1 LOC_Os03g49900 Chromosome
segment substitution
lines
Map-based
cloning
RING-type E3 ligase Positive
regulation
Ubiquitinate TT3.2
for vacuolar
degradation
CG14 InDel, CAPS one amino acid substitution (Zhang et al., 2022)
OgTT3.2 LOC_Os03g49940 Chromosome
segment substitution
lines
Map-based
cloning
Chloroplast precursor
protein
Negative
regulation
Accumulation under
HS cause chloroplast
damage
CG14 InDel, CAPS one amino acid substitution (Zhang et al., 2022)
Shen et al. 10.3389/fpls.2022.1021203
Frontiers in Plant Science frontiersin.org07

rice under the current climate conditions has become one of the
important objectives of breeding. At present, the related genes
successfully cloned are limited, which makes it difficult to
cultivate heat-resistant rice. Therefore, it will be one of the key
problems for future research to apply heat-resistant genes to
breeding practice. Moreover, because most of the current studies
have little relationship with rice yield traits, different genes/QTLs
affecting yield and heat tolerance have to be considered
simultaneously in the breeding process, which undoubtedly
increases the burden of breeding work and extends the
breeding period. It is expected that how to strengthen the
relationship between heat tolerance and rice yield will be an
important issue to be solved in the future to improve
breeding efficiency.
Author contributions
QS and YX jointly wrote this mini review, XQ helped to
revise the manuscript, and JY conceived and guided the writing
of the manuscript.
Funding
This work was financially supported by grants from the National
Natural Science Foundation of China (32171931) and the open
project from State Key Laboratory of Rice Biology (160102) to JY.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.
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