Plant Cell Rep (2014) 33:551–564

DOI 10.1007/s00299-013-1551-x

REVIEW

Recent progress on molecular breeding of rice in China

Received: 22 November 2013 / Revised: 9 December 2013 / Accepted: 10 December 2013 / Published online: 19 January 2014
Ó The Author(s) 2014. This article is published with open access at [Link]

Abstract Molecular breeding of rice for high yield, century. The first breakthrough is the development of a
superior grain quality, and strong environmental adapt- semi-dwarf rice variety in the 1960s, which raised rice yield
ability is crucial for feeding the world’s rapidly growing by more than 20 % per unit area; the second breakthrough is
population. The increasingly cloned quantitative trait loci the development of a hybrid rice variety with the three-line
and genes, genome variations, and haplotype blocks related or cytoplasmic male sterile system in the 1970s, which led
to agronomically important traits in rice have provided a to another great increase in average rice yield by 20 %
solid foundation for direct selection and molecular breed- (Yuan 1987). The previous achievements have contributed
ing, and a number of genes have been successfully intro- greatly to the self-sufficiency in China’s food supply.
gressed into mega varieties of rice. Here we summarize Thereafter, however, no substantial progress has been made
China’s great achievements in molecular breeding of rice in improving rice yield. In 1986 and 1996, International
in the following five traits: high yield, biotic stress resis- Rice Research Institute and China launched the Super Rice
tance, abiotic stress resistance, quality and physiology. Breeding Program to fight in stages for increasing rice yield.
Further, the prospect of rice breeding by molecular design Recently, rapid economic development and population
is discussed. growth have placed heavy pressure on crop production in
China. To meet the security of food supply, we must
Keywords Molecular breeding
Marker-assisted increase the crop yield per unit area by 50 % before 2030
selection
Breeding design
Agronomic traits
Rice (Cheng and Hu 2008). In this context, it is imperative to find
breeding new applicable methods for rice breeding.
Conventional breeding selects genotypes indirectly
through phenotypes, which is generally effective for qual-
Introduction itative traits only but not for quantitative traits. It is due to
that quantitative traits with continuous variations are con-
Rice is one of the most important staple crops in the world trolled by multiple genes and environmental factors. Over
and serves as a model for monocots. In rice breeding, two the past few decades, advances of molecular markers,
breakthroughs have been made in China over the last transgenic technology, and genomics have exerted far-
reaching influences on the concept and means of conven-
tional rice breeding, allowing applications of molecular
Communicated by N. Stewart. breeding technology in rice. Molecular breeding refers to
the development of new rice varieties by integrating the
Y. Rao
Y. Li
Q. Qian (&)
State Key Laboratory of Rice Biology, China National Rice means of modern biotechnology into conventional breeding
Research Institute, Hangzhou 310006, China methods (Fig. 1), which mainly involve marker-assisted
e-mail: qianqian188@[Link] selection (MAS) and genetic engineering breeding (GEB).
Compensating the deficiencies of conventional breeding,
Y. Rao
College of Chemistry and Life Sciences, Zhejiang Normal molecular markers designed for direct genotypic identifi-
University, Jinhua 321004, China cation are unrestricted to the ontogenetic periods of plants

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Fig. 1 The scheme of applying

and can be used to select target traits directly. MAS Multiple chromosome segment substitution lines are con-
involves four steps: overall program design, selection of structed, and a large number of QTLs are identified. Many
target genes and parental materials, construction of breeds carrying objective QTLs or genes are applied in rice
breeding populations, and molecular marker screening of production (Table 1), and an increasing number of rice
early generation materials. The breeding process of MAS is varieties and genetic populations are sequenced, laying a
similar to that of conventional breeding, except that in the foundation for rice breeding by molecular design. Here we
former method, molecular marker detection is involved in summarize China’s current situation of molecular breeding
every breeding generation on the basis of conventional in rice regarding different traits, and further discuss the
phenotypic identification. prospects of rice breeding by molecular design (MDB).
GEB of rice mainly involves in vitro recombination of a
specific target gene with the transformation vector, fol-
lowed by transferring into rice for stable integration, Molecular breeding for high yield
expression, and heredity. This breeding method avoids the
impacts of adverse genes caused by genetic linkage in the High yield is the eternal theme pursued by rice breeders.
process of sexual hybridization and gets rid of reproductive Super rice breeding in the model of ideal plant architecture
isolation between different rice cultivars. Therefore, GEB using molecular design is the mainstream of future devel-
provides an efficient way for cultivating new rice varieties. opment in this field. Yield-related traits in rice include
In recent years, great efforts have been made in rice plant height, tiller number, grain weight, and panicle type.
genome sequencing and there have been significant Of these, plant height is the most important trait related to
developments of functional genomics. The increasingly plant architecture and linearly correlates with biomass.
cloned quantitative trait loci (QTL)/genes, genome varia- Panicle number, which consists of planting density and
tions, and haplotype blocks related to agronomically effective tiller number, is a major influencing factor of the
important traits in rice provide a solid foundation for direct total grain production per unit area. Panicle characters are
selection and molecular breeding of rice. A number of directly linked with the yield of rice (Xing and Zhang
genes are successfully transferred into mega rice varieties. 2010). Recently, multiple yield-related genes and QTLs

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Table 1 Examples of marker-assisted selection (MAS) and genetic engineering breeding (GEB) in rice
Varieties/lines Types Genes involved Donors Tolerance to/ Breeding Code/reference
exploited traits methods

Zhonghui 8006 Indica Xa21, GM6 Duoxi 1, Minghui 63 BB, GM MAS CNA20030473.9
Zhonghui 218 Indica Xa21 IRBB 21 BB MAS CNA20030093.8
Guodao 1 Indica Xa21 Zhonghui 8006 BB MAS CNA20050721.4
Guodao 3 Indica Xa21 Zhonghui 8007 BB MAS Cao et al. (2006)
Guodao 6 Indica Xa21 Zhonghui 8008 BB MAS CNA20050722.2
IIYou 8006 Indica Xa21 Zhonghui 8006 BB MAS Wu et al. (2008c)
IIYou-218 Indica Xa21 Zhonghui 218 BB MAS CNA20060721.9
Yuanhui 611 Indica yld1.1, yld2.1 O. rufipogon High yield MAS CNA20030432.1
Y-You 7 Indica yld1.1, yld2.1 Yuanhui 611 High yield MAS Wu et al. (2010a)
RB207-1 Restorer Barnyardgrass Genomic DNA High yield GEB CNA20030177.2
Shuhui 527 Restorer Xa4, Xa21 1318/88-R3360 BB MAS CNA20000073.X
Zhunliangyou 527 Indica Xa4, Xa21 Shuhui 527 BB MAS CNA20030033.4
D-You 527 Indica Xa4, Xa21 Shuhui 527 BB MAS CNA20010111.0
Xieyou 527 Indica Xa4, Xa21 Shuhui 527 BB MAS CNA20030434.8
RGD-7S/RGD-8S CMS Pi1, Pi2 BL122 RB MAS Liu et al. (2008b);
Yueza 746/763 Indica Pi1, Pi2 RGD-7S RB MAS Jin et al. (2007)
W3660 Japonica Lgc-1 LGC-1 Low glutelin content MAS CNA20020113.1
W017 Japonica Lox3 DawDam Prolonged storage of seeds MAS CNA20020290.1
W025 Japonica ge Haiminori Huge embryo MAS CNA20030548.4
Huahui 1 Restorer Cry1Ac/Cry1Ab Minghui 63 Insects GEB Liu et al. (2012)
Zhonghui 161 Restorer Pita, xa13, wx IRBB 51, Teqing RB, BB, good quality MAS CNA20060673.5
Bph68S/Luohong4A CMS Bph14, Bph15 B5 BPH MAS Zhu et al. (2013)
Ning 9108 Indica Stv-bi, Wx-mq Guandong 194 Strip blight, good quality MAS Yao et al. (2010)
T16S GMS Bt Minghui 63 Insects GEB Wu et al. (2010b)
BB, bacterial blight; RB, rice blast; GM, gall midge; BPH, blight planthopper; Bt, Bacillus thuringiensis; MAS, marker-assisted selection
breeding; GEB, genetic engineering breeding

have been identified and cloned in rice (Table 2), providing segment substitution line that has genetic background of
a good opportunity for molecular breeding with greater Huajingxian 74 and carries the grain length genes GS3 and
potential of rice yield. GW8 with other excellent genes. Recently, the character-
In 1991, the high-stem gene eui was first transferred into istics of panicle size have been improved significantly by
the widely used sterile line Zhenshan 97A by MAS. In the clustering 8 panicle number and weight-related QTLs via
following year, this gene was transferred into other sterile MAS (Zong et al. 2012). Meanwhile, the strong restorer
lines using the backcrossing method to overcome the issue line Q611 and the hybrid rice variety Y-You-7 were
of elongated internodes of sterile lines (Liang et al. 1992). obtained by transferring two high-yield genes of the
Recently, the dense and erect panicle 1 (DEP 1) gene, Malaysian wild rice Oryza rufipogon, yld1.1 and yld2.1
closely related to plant type, has been cloned (Huang et al. (Wu et al. 2010a), into the elite restorer lines Ce64-7 and
2009). Using an elite indica variety (curved panicle type 9311 via MAS (Table 1).
Nanhui 602) as female parent and a NIL-DEP1 DW135 as In 2003, the State Key Laboratory of Rice Biology
male parent, researchers carried out MAS of backcross (SKLRB) of China National Rice Research Institute
population, screened out a DEP1-containing homozygous (CNRRI) cooperated with the research group of Acade-
line, and further investigated panicle traits in heading date; mician Li Jiayang from Chinese Academy of Sciences to
the results were consistent with molecular marker detection complete the cloning of rice monoculm 1 (MOC1) gene (Li
data, providing a theoretical reference and materials for et al. 2003). With the help of MOC1 cloning, the SKLRB
future plant architecture breeding (Cheng et al. 2011). of CNRRI launched a research project funded by the 863
Yang et al. (2010) and Wang et al. (2012b) effectively program, Creation and Applications of Super High-yield-
improved the grain size and the exterior quality of an ing Germplasm of MOC1 Transgenic Rice. This project
indica variety, Huajingxian 74, by molecular pyramiding mainly aimed to transfer sense, antisense, and deletion
breeding, which involved the hybridization of a single genes of MOC1 into mega variety and the parents of hybrid

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Table 2 Map-based cloning of genes using mutants or QTL as a tool involved in rice high yield in recent years
Trait QTL or QTL/gene RAP-DB Encoded product Reference
mutant

Plant architecture mutant HTD2 Os03g0203200 Putative esterase Liu et al. (2009)
mutant OsCD1 Os12g0555600 Cellulose synthase Luan et al. (2011)
mutant OsGA2ox6 Os04g0522500 Gibberellin 2-oxidase Huang et al. (2010)
QTL IPA1/WFP Os08g0509600 Squamosa promoter binding protein-like 14 Jiao et al. (2010)
QTL OsPH1 Os01g0881500 Chitin-inducible gibberellin-responsive protein Kovi et al. (2011)
mutant LAZY1 Os11g0490600 Expressed protein Li et al. (2007)
mutant PROG1 Os07g0153600 Cys2-His2 zinc finger protein Jin et al. (2008)
mutant DLT Os06g0127800 GRAS family protein (involved in brassinosteroid) Tong et al. (2012)
Panicle characters mutant EUI1 Os05g0482400 Cytochrome P450 monooxygenase Zhang et al. (2008)
mutant sui1 Os01g0118300 Phosphatidyl serine synthase Zhu et al. (2011)
mutant SP1 Os11g0235200 Peptide transporter Li et al. (2009b)
mutant LAX2 Os04g0396500 Nuclear protein with a plant-specific conserved domain Hiroaki et al. (2011)
QTL Ghd7 Os07g0261200 CCT -domain protein Xue et al. (2008)
mutant DEP2/SRS1 Os07g0616000 Novel plant-specific protein Li et al. (2010a)
mutant LAZY1 Os11g0490600 Specific herb protein Chen et al. (2012)
mutant EG1 Os01g0900400 Lipase Li et al. (2009a)
QTL DTH8/Ghd8 Os08g0174500 OsHAP3 subunit of a CCAAT-box-binding protein Wei et al. (2010)
QTL DEP1/qPE9- Os09g0441900 PEBP-like domain protein Huang et al. (2009)
1
mutant DEP3 Os06g0677000 Patatin-like phospholipase A2 protein Qiao et al. (2011)
mutant OsPIN2 Os06g0660200 Auxin efflux transporter Chen et al. (2012)
Grain QTL GS3 Os03g0407400 Transmembrane protein Yang et al. (2010)
QTL Gn1a Os01g0197700 Cytokinin oxidase/dehydrogenase Li et al. (2013)
QTL GS5 Os05g0158500 Serine carboxypeptidase Li et al. (2011b)
QTL GW2 Os02g0244100 RING-type E3 ubiquitin ligase Song et al. (2007)
QTL GW5 Os05g0187500 Novel nuclear protein Weng et al. (2008)
QTL GW8 Os08g0531600 Squamosa promoter binding protein-like 16 Wang et al. (2012b)
Tiller mutant MOC1 Os06g0610350 GRAS family nuclear protein Li et al. (2003)
QTL TAC1 Os09g0529300 Unknown Jiang et al. (2012)
Heading and mutant HGW Os06g0160400 Ubiquitin-associated domain protein Li et al. (2012b)
grain weight
Grain filling QTL GIF1 Os04g0413500 Cell wall invertase Wang et al. (2010a)
Shattering QTL SHA1 Os04g0670900 Plant-specific transcription factor Lin et al. (2007)

rice for changing MOC1 expression level and regulating MOC1-containing breeding materials from different gen-
rice tiller numbers. erations were obtained by transformation, including 40
In addition, GEB has been applied for screening trans- intermediate materials from advanced lines.
genic plants with less or no tillers, good agronomic traits, Previous work indicates that using modern genetic
and great potential for high yield. To date, more than 50 engineering technology, we are able to obtain transgenic
transgenic lines have been bred using the pedigree methods plants with fewer tillers, high nutrient contents, and supe-
and 30 transgenic intermediate materials are obtained. Of rior agronomic traits in super rice breeding. The gradient
these, three transgenic varieties were further selected for tiller materials generated by transgenosis are expected to
significantly improved production and potential for appli- provide a new platform for exploring the theory and
cation compared to the control lines; four lines with fewer technology of super rice breeding. With the cloning of
tillers were used for variety demonstration; and some lines IPA1, great breakthroughs have been made in under-
were used as intermediate materials. In addition, MOC1 standing the mechanism of ideal plant architecture in rice.
transgenic pure lines were hybridized with conventional It has been reported that IPA1 contributes mostly to more
varieties such as Zhi-7 and Zhongchao-123, and a series of panicles, strong culms, and high-yield potential. This gene

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has been transferred into the rice cultivar Xiushui 11 multiple disease-resistant varieties (Deng et al. 2005). In
through backcross breeding and the obtained mutant lines recent years, these rice varieties have been applied in rice
exhibit ideal plant architecture with a 10 % increase in the production in an average annual area of approximately
yield in field experiments (Jiao et al. 2010). 35,000 hm2, which are considered to be successful exam-
In overseas, great achievements also had been acquired. ples for commercial application of bacterial blight resis-
Previously, the plant height gene sd1 was transferred from tance genes.
the variety Habataki into the variety Koshihikari using Using MAS, Wang et al. (2004b) transferred two bac-
MAS; near-isogenic lines NIL-GN1 ? sd1, a kind of semi- terial blight resistance genes, Xa21 and Xa4, into restorer
dwarf, large-panicle, high-yielding lines, were constructed lines, bred the disease-resistant, high-affinity restorer line
(Ashikari et al. 2005), providing a new pathway for the Shuhui 527, and configured a combination of two-line
green revolution in rice. hybrid rice Zhunliangyou 527 and three-line hybrid rice D
You 527, Gangyou 527, and Xieyou 527 (Table 1). In
addition, Liu et al. (2008b) and Jin et al. (2007) transferred
Molecular breeding for resistance to biotic stress Xa7 into three-line restorer lines and bred the restorer lines
Guanghui 806 and Guanghui 312. Pi-1 and Pi-2 were also,
In rice production, biotic stress mainly refers to plant dis- respectively, transferred into the sterile lines GD-7S and
eases and pests. The major rice diseases are fungal, bac- GD-8S for breeding the new sterile lines RGD-7S and
terial, and viral diseases and rice blast. Serious losses to RGD-8S (Table 1) for high resistance to rice blast, and new
rice production are commonly caused by more than 70 combinations of two-line hybrid rice with high resistance
diseases, of which rice blast, sheath blight, and bacterial to rice blast were screened out, including Yueza 746, Yu-
blight are most harmful to rice. In addition, rice is one of eza 751, Yueza 4206, and Yueza 750.
the crops suffering from most pests’ attacks. There are On the other hand, gene loci were detected in segregating
more than 624 insect species in field harmful to rice, of generations of Wuyunjing 8 and Zhendao 42 using gene
which planthopper, leafhopper, and stemborer cause the markers of Pi-ta and Pi-b and molecular markers tightly
most serious hazards and lead up to 32 % yield losses in linked with Stv-bi; the three disease resistance genes were
rice (Pei et al. 2011). Controlling of the pests and breeding transferred simultaneously into high-yield varieties to breed a
of disease-resistant varieties have long been the focus of high-yield, good-quality, and multi-resistance new rice line,
rice research. In China, a number of exploratory studies 74121, by a combination of multi-generation breeding in field
have been conducted on plant disease resistance in rice, with resistant gene identification (Wang et al. 2011). In
and a series of relevant genes (e.g., Xa21) have been cloned another study, the rice blast resistance gene Pi-1 was trans-
and applied in rice production (Table 3). These works have ferred into the three-line sterile line Jinkang A (Guan et al.
greatly promoted rice breeding for high resistance to biotic 2009). Recently, continuous breakthroughs have been made
stress by MAS and GEB. in molecular breeding of rice for resistance to stripe diseases.
Bacterial blight and rice blast resistance genes are most Pyramiding breeding was carried out by configuring hybrid
commonly used in rice breeding for disease resistance. combinations between the Jiangsu high-yielding rice variety
Since the bacterial blight-resistant gene Xa21 is tightly Wuyunjing 7 as female parent and the Japanese japonica
linked to the molecular marker PTA248, researchers from variety Guandong 194 (containing the stripe disease resis-
CNRRI detected homozygous-resistant plants using the tance gene Stv-bi and dark endosperm mutant gene Wx-mq) as
molecular marker in the offspring of a cross of Xa21- male parent to breed new disease-resistant rice lines with
containing variety IRBB21 and non-Xa21-containing good cooking quality (Yao et al. 2010).
variety IR24; two Xa21-carrying restorer lines, Zhonghui In rice molecular breeding for high resistance to pest,
8006 and Zhonghui 218 (Table 1), were bred, and a series the elite two-line restorer line Yangdao 6 was hybridized
of super rice combinations were obtained, such as Guodao with a selectable marker-eliminated Bt transgenic restorer
1 (Cao et al. 2005), Guodao 3 (Cao et al. 2006), Guodao 6 line Minghui 63 to breed the transgenic pest-resistant
(Wu et al. 2008b), and II You 8006 (Wu et al. 2008c). In photo-thermo-sensitive genic male sterile line T16S (Wu
addition, maintainer lines pyramiding three rice blast et al. 2010b). In 2013, the Honglian-type new sterile line
resistance genes (Pi-1, Pi-2, and Pi-33) and maintainer and Luohong 4A resistant to brown planthopper (BPH) was
restorer lines pyramiding a rice blast resistance gene (Pi- bred in Wuhan University by a combination of MAS and
25) with two bacterial blight resistance genes (Xa-23 and conventional breeding; Luohong 4A demonstrated signifi-
Xa-21) were created. With the help of MAS, new resistance cant BPH resistance by pyramiding two BPH-resistant
rice lines pyramiding multiple bacterial blight resistance genes, Bph14 and Bph15 (Zhu et al. 2013).
genes (Xa4, Xa13, and Xa21) were screened out from the Xiao et al. (2005) transferred the rice gall midge
offspring of a cross between the variety IBRR60 and (RGM)-resistant gene Gm6 into the restorer lines Gui99

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Table 3 Major important genes tagged and mapped with molecular markers in rice for biotic stresses in recent years
Biotic stress Gene Donor Chr. Linked marker Reference

Bacterial blight Xa13 IRBB13 8 R2027 (1.3 cM), RG136(2.3 cM) Li et al. (2012a)
Xa4 IRBB4 11 R1506, s12886 (0.5 cM) Deng et al. (2005)
Xa7 IRBB7 6 G1091 (6.0 cM), AFLP31-10 (3 cM) Porter et al. (2003)
Xa21 O. longistaminata 11 RG103 (0 cM) Gan et al. (2011)
Xa22(t) Zhachanglong 11 RG103 (0 cM) Pei et al. (2011)
Xa23 O. rufipogon 11 C1003A (0.4 cM) Chen et al. (2009)
xa24 DV85, DV8, Aus 295 2 RM14222 (0.07 cM), RM14226 (0.07 cM) Wu et al. (2008d)
Xa25(t) Minghui63 12 G1314 (7.3 cM), R887 Pei et al. (2011)
Xa29 O. officinalis 1 C904, R596 Tan et al. (2004)
xa32(t) Y76 12 RM8216 (6.9 cM)–RM20A (1.7 cM) Ruan et al. (2008)
xa34(t) BG1222 1 RM10929, BGID25 Chen et al. (2011b)
Rice blast Pi1 LAC23 11 RZ536 (7.9 cM), Npb181 (3.5 cM) Hua et al. (2012)
Pi2/Pi9 5173 6 RG64 (0.9 cM), AP22 (1.2 cM) Zhu et al. (2012)
Pi9(t) Oryza minuta 6 Pb9-1 Chen et al. (2009)
Pid3/Pi25 Gumei2 6 A7 (1.7 cM), RG456 (1.5 cM) Chen et al. (2011a)
Pi33 IR64 8 Y2643L (0.9 cM), RM72 (0.7 cM) Miah et al. (2013)
Pik-p K60 11 RM5926-K37 Yuan et al. (2011)
Pi41 Nov-93 12 STS40-1–STS40-3 Yang et al. (2009b)
Pid(t) Digu 2 G1314A (1.2 cM), G45 (10.6 cM) Pei et al. (2011)
Brown planthopper Bph6 Swarnalata 11 RM6997–RM5742 Qiu et al. (2010)
Bph14 O. officinalis 3 G1318–R1925 Zhu et al. (2013)
Bph19(t) AS20- 1 3 RM6308–RM3134 Chen et al. (2006)
White-backed Wbph6(t) Guiyigu 11 RM167–RM287 Li et al. (2010a, b)
planthopper
Gall midge GM6 Duokang1 4 PSM101, PSM106, PSM115 Xiao et al. (2005)
Stripe disease stv-bi 11 ST10 Yao et al. (2010)
Insects Bt Bacillus thuringiensis Chen et al. (2009)

and Guanghui 998 using the gene marker PSM101 and pure line with comparable resistance to specific biotic
preliminarily bred the RGM-resistant restorer lines KG18-1 stresses mentioned above (Chen et al. 2009). In addi-
and KG18-2. In September 2009, the Ministry of Agri- tion, two anti-aging genes (IPT and Xa23) and a rice
culture issued a security certificate to the cry1Ab/cry1Ac blast resistance gene (Pib) were pyramided into the
transgenic insect-resistant rice Huahui 1 and Bt Shanyou 63 same lines to obtain anti-aging, bacterial blight-resis-
for production permissions in Hubei Province (Liu et al. tant, and rice blast-resistant intermediate materials for
2012). Scientists from Science Academy of China created crossbreeding (He et al. 2004).
new-type pest-resistant transgenic materials and carried out
bio-safety evaluations for non-selectable marker sck/
cry1Ac double gene insect-resistant transgenic rice lines, Molecular breeding for resistance to abiotic stress
derived varieties, and their hybrid combinations. Zhang
et al. (2013b) created three copies of new restorer materials Abiotic stress of rice is collectively referred to natural
containing the major QTLs, qSI4, of anti-feeding resistance adversity and artificial adversity. Natural adversity includes
to white-backed planthopper by a combination of MAS and meteorological disasters (e.g., floods, droughts, typhoons,
conventional breeding. and cold damage) and soil adversity (e.g., salt damage);
For cultivating new rice varieties resistant to both artificial adversity is mainly human-induced environmental
plant diseases and pests, multi-gene pyramiding pollution. In recent years, molecular breeding for abiotic
breeding has been carried out. For example, genes stress tolerance in rice has been developed significantly,
highly resistant to bacterial blight (Xa23), rice blast and a series of genes and QTLs have been identified for
(Pi9), and rice stem borer and leaf roller (Bt) were their high application potential in rice breeding for resis-
pyramided into the same lines using MAS to obtain a tance to adversity (Table 4).

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Table 4 Major important genes tagged and mapped with molecular markers in rice for abiotic stress, quality, physiology and hybrid traits in
recent years
Trait Gene RAP-DB Encoded product Gene function Reference

Abiotic OsTPP1 Os02g0661100 Trehalose-6-phosphate phosphatase Tolerance to salt and cold Ge et al. (2008)
resistance OCPI1 Os01g0615100 Chymotrypsin inhibitor Tolerance to drought Huang et al. (2007)
LTN1 Os05g0557700 Ubiquitin–conjugating domain Signal of Pi starvation Hu et al. (2011)
protein
OsLEA3-1 Os05g0542500 Late embryogenesis abundant Tolerance to drought Xiao et al. (2007)
protein
OsPht1 Os10g0444700 Phosphate transporter Absorption and transport of Pi Jia et al. (2011)
OsSKIPa Os02g0759800 Unknown Tolerance to drought Hou et al. (2009)
LOX3 Os03g0700400 Lipoxygenase Tolerance to various stress Liu et al. (2008a)
OsCOIN Os01g0104100 Zinc finger protein Tolerance to salt, cold and drought Liu et al. (2007b)
OsHAL3 Os06g0199500 Halotolerance protein Tolerance to salt Sun et al. (2009)
SKC1 Os01g0307500 Na?-selective transporter Tolerance to salt Ren et al. (2005)
SNAC2 Os01g0884300 Nuclear protein Tolerance to salt and cold Hu et al. (2008)
Quality OsVPE1 Os04g0537900 Vacuolar processing enzyme Maturity of gluten Wang et al. (2009b)
RSR1 Os05g0121600 Unknown Regulating starch synthesis of seeds Fu and Xue (2010)
OsRab5a Os12g0631100 Small GTPase Transporting storage protein Wang et al. (2010b)
ALK Os06g0229800 Soluble starch synthases Regulating gel temperature Gao et al. (2003)
qGC-6(wx) Os06g0133000 Granule-bound starch synthase Regulating amylase content Su et al. (2011)
OsBADH2/fgr Os08g0424500 Betaine aldehyde dehydrogenase Fragrance Chen et al. (2008)
Physiology Phr1 Os04g0624500 Polyphenol oxidase Browning seeds Yu et al. (2008)
OsMST6 Os07g0559700 Monosaccharide transporter Regulating grain filling Wang et al. (2008)
SLL1 Os09g0395300 KANADI Transcription Factor Regulating leaf morphology Zhang et al. (2009)
LC2 Os02g0152500 Unknown Regulating leaf angle and flowering Wang et al. (2013)
Roc5 Os02g0674800 Leu-chain-like protein Regulating leaf morphology Zou et al. (2011)
NLS1 Os11g0249000 Typical CC-NB-LRR domain Resistance to pathogens Tang et al. (2011)
protein
SL1 Os01g0129200 Z-finger domain protein Regulating rice floral development Xiao et al. (2009)
NRL1/ Os12g0555600 Cellulose synthase Cell-wall synthesis and plant growth Yoshikawa et al. (2013)
OsCSLD4
Physiology OsRAA1 Os01g0257300 12 kDa small G protein Regulating root growth Han et al. (2008)
WOX11 Os07g0684900 Unknown Regulating root growth Zhao et al. (2009)
OsC6 Os11g0582500 Lipid transfer protein Involving in anthers development Zhang et al. (2010b)
OsPSS1 Os04g0573000 Pi-transport protein Involving in Pi balance of leaves Wang et al. (2012a)
PTC1 Os09g0449000 PHD-Finger Protein Involving in anthers development Li et al. (2011a, b)
OsJAG Os01g0129200 C2H2 Z-finger domain protein Involving in floral development Duan et al. (2010)
CYP704B2 Os03g0168600 Cytochrome P450 Regulating anther and pollen formation Li et al. (2010b)
OsMST4 Os03g0218400 Monosaccharide transporter Regulating sugar distribution Wang et al. (2007)
OsYABBY4 Os02g0643200 YABBY-domain protein Expressing in vascular tissues Liu et al. (2007a)
SDG714 Os01g0927000 Histone H3K9 methyl-transferase Regulating leaf morphology Ding et al. (2007a)
OsAGO7 Os03g0449200 Argonaute (AGO) protein Regulating leaf morphology Shi et al. (2007)
RID1 Os10g0419200 Cys2/His2 type z-finger Regulating reproductive growth Wu et al. (2008a)
transcription factor
S5 Os06g0213100 Aspartic protease Regulating reproductive isolation Ji et al. (2012)
Sa Os01g0578700 Small ubiquitin-like modifier E3 Regulating male sterility Long et al. (2008)
ligase-like protein/F-box protein
EUI1 Os05g0482400 Cytochrome P450 monooxygenase Hybrid rice pollination Zhang et al. (2008)
CYP714D1
OsUgp1 Os09g0553200 UDP-glucose pyrophosphorylase Male fertility Chen et al. (2007)
CSA Os01g0274800 R2R3-type MYB transcription Mutation causing sensitive male sterility Zhang et al. (2013a)
factor
orfH79 Mitochondria Cytotoxic peptide Regulating in HL-CMS Peng et al. (2010)
COX11 Os03g0718600 Nuclear-encoded mitochondrial Interacting with WA352 Luo et al. (2013)
protein
WA352 Mitochondria Unknown Regulating in WA-CMS
Rf5/Rf1 Os10g0497300 PPR protein Restoring fertility of BT-CMS Hu et al. (2012)

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Drought resistance is a complex trait in plants, which studies have attempted to enhance cold tolerance of rice by
refers to the tolerance of plants to water-deficient envi- molecular breeding. This is probably because cold toler-
ronment. The existing technical evaluation and standards ance in rice is a cumulative trait regulated by multiple
for drought resistance cannot reflect the actual growth genes, and single-gene transformation techniques have
conditions of plants accurately. In China, studies have been limited efficiency in improving rice cold tolerance.
reported on QTL mapping of drought resistance traits in Salt damage is one of the important causes for decline in
rice and a number of relevant genes cloned (Table 4). Eight rice yield and saline-alkali soil covers an area of approxi-
QTL for rice root traits were identified in the doubled mately 100 million hm2 in China (Hu et al. 2010). To date,
haploid (DH) lines Zhaiyeqing 4 and Jingxi 17 (Xu et al. a few genes for salt tolerance have been cloned (Table 4)
2001), and two drought-tolerant QTL, qDT5 and qDT12, and breeding practices for salt resistance have been carried
were detected at seedling stage and located at GA41– out using GEB. In 2006, the salt tolerance gene OPBP1
GA257 on chromosome 5 and RG457–Y12817R on chro- was transferred into rice using a gene gun method and the
mosome 12 (Teng et al. 2002). Drought-tolerant QTLs obtained transgenic plants showed faster growth with sig-
including root traits (diameter, length, weight, and root/ nificantly higher chlorophyll content and biomass yield
shoot ratio), leaf water potential and osmotic potential, as than the non-transgenic control (Li and Guo 2006). The
well as plant height, stem diameter, and flag leaf length and rice HAL2-like gene (RHL) was transferred into the
width were identified in DH lines of two japonica rice japonica variety Hejiang 19 using an Agrobacterium-
varieties, IRAT 109 and Yuefu, under different environ- mediated method, and the screened positive plants showed
mental conditions (root irrigation, potted paddy field, and improved salt tolerance at the seedling stage with less
dry land); in total, 21 additive QTL and 23 pairs of epistatic damage to cell membrane, strong vitality of leaf tissues,
QTL were detected, and environmental interaction was and enhanced salt tolerance under salt stress at the booting
detected in QTLs of root number, root fresh weight, root stage (Hu et al. 2010). The 2-pyrrol 5-carboxylate synthase
dry weight, and root/shoot ratio, but not in QTLs of basal (P5CS) gene from leguminous plants was transferred into
root thickness, maximum root length, fresh stem weight, or rice using the gene gun method and the transgenic plants
dry stem weight; overall, the QTLs controlling fresh and obtained increased content of proline with enhanced salt
dry root weights had the most significant interactions with tolerance in transgenic cells (Zhi et al. 2005). In addition,
the environment, accounting for 26 and 28 % of the vari- transgenic rice plants with enhanced salt tolerance were
ance, respectively (Mu et al. 2003). In addition, drought- obtained by transferring single genes such as 1-phosphate
related QTLs such as those associated with fresh root mannitol dehydrogenase (mtlD) gene and 6-phosphate,
weight and leaf water potential were identified in different sorbitol dehydrogenase (gutD) gene, or double genes such
populations of recombination inbred lines (RILs) in paddy as choline monooxygenase (CMO) gene/betaine aldehyde
field and dry land (Qu et al. 2008). Knowledge of these dehydrogenase (BADH) gene into rice varieties (Hu et al.
QTLs will benefit MAS breeding of rice for drought 2010).
resistance. In 2006, Guo et al. (2006) transferred five salt tolerance-
Cold damage of rice occurs at the budding, seedling, related genes, CMO, BADH, 1-phosphate mannitol dehy-
booting, flowering, and grain filling stages. Of these, anti- drogenase (mtlD) gene, gutD, and S-adenosylmethionine
cold stress in the seedling stage is the focus of relevant decarboxylase (SAMDC) gene, into the conventional
research. QTLs related to cold stress have been identified japonica varieties Xiushui 11 and Zhonghua 11, indica
with different methods (Table 4). Backcross generation varieties Teqing and hybrid restorer line Minghui 63 using
was analyzed in 213 lines of Xieqingzao B and Dongxiang Agrobacterium-mediated and gene gun methods; the five
wild rice with the seedling mortality rate at low tempera- salt tolerance genes were then pyramided through con-
ture as an indicator; it was found that the seedling mortality ventional cross breeding and the rice line Xiushui 11 with
rate was continuously distributed in the population, that is, nine genotypes was bred; further, these rice lines were
cold tolerance is a quantitative trait controlled by multiple chosen for comprehensive evaluation and effective utili-
genes; further, the major effect QTL was found on chro- zation in south Zhejiang Province. Using map-based
mosome 8 in rice (Rao et al. 2013). cloning, Ren et al. (2005) isolated the gene SKC1 that is
Wang et al. (2009c) investigated a set of RILs using the involved in regulating K(?)/Na(?) homeostasis under salt
germination rate under low-temperature stress as an indi- stress, providing a potential tool for improving salt toler-
cator and detected seven QTLs for cold tolerance on ance in crops.
chromosomes 4, 6, and 9 in rice. The majority of known In China, few studies have investigated submergence
QTLs for cold tolerance are mainly located on chromo- stress in rice. New submergence-tolerant germplasm such
somes 4 and 8, accounting for 16.22 and 13.51 % of the as 94D-05, 94D-34, and 94D-54D have been obtained
total QTLs, respectively (Rao et al. 2013). At present, few using an exogenous DNA introduction method, and the

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varieties Guizhao 2, Hui 41, 8105/D100, and Shanyou 63 potential. In China, a number of rice genes related to
with strong submergence tolerance were screened out physiological traits have been cloned (Table 4). These
under artificial simulation conditions (Li and Li 2000). genes have been used in molecular breeding of rice for
high-photosynthetic efficiency as a new means of physio-
logical breeding, relative to rice breeding of plant archi-
Molecular breeding for rice grain quality tecture in the 1960s. The focus of rice breeding for high-
photosynthetic efficiency is to explore potential of the
Rice quality, as jointly determined by the appearance, single-leaf photosynthetic rate.
processing, cooking, eating, and nutrition of rice, is the C4 plants are considered to have higher photosynthetic
characteristic of rice commercialization and industrializa- efficiency than C3 plants by lower photorespiratory con-
tion. In China, many genes and QTLs related to rice quality sumption. Phosphoenolpyruvate carboxylase (PEPCase) is
have been cloned (Table 4), and some genes are used in the key enzyme for CO2 fixation in C4 plants. A maize
practices of breeding. PEPC gene was transformed into rice variety to produce
Using MAS with the functional marker GRM04, new new transgenic rice materials. Scholars have investigated
hybrid rice materials with strong fragrance were bred in the possible mechanisms of unique CO2 assimilation and
Guangdong Academy of Agricultural Sciences by intro- high-photosynthetic efficiency in the rice variety carrying
ducing fragrant (fgr) gene into the three-line maintainer PEPC; high-yielding rice plants with stable high-photo-
lines Tianfeng B, Rongfeng B, Taifeng B, and Zhenfeng B synthetic efficiency were obtained by system selection and
as well as the elite restorer lines Guanghui 998, Guanghui multi-generation cultivation; finally, high-yielding rice
290, and Guanghui 372. New wx-containing rice lines with varieties with high-photosynthetic efficiency were bred (He
low content of amylose were developed (1.36 % in D154, et al. 2005). The attempts of rice breeding for high-pho-
14.28 % in D156, and 13.13 % in D174 vs. 26.8 % in tosynthetic efficiency by a combination of conventional
Tianfeng B). breeding and molecular biotechnology provide new
Hybrid combinations were configured for pyramid approaches for breeding super rice in the future.
breeding using Wuyunjing 7 as female parent and the Stv- Physiological analysis demonstrated that PEPCase
bi- and Wx-mq-carrying Guandong 194 as male parent; the activity of Kitaake-PEPC transgenic rice varied in the til-
marker SCAR co-segregated with Stv-bi and the functional lering and heading stages, as well as different growth
marker CAPS linked to Wx-mq were used to detect the stages of flag leaf, all significantly higher than that in the
target loci in segregating generations; Stv-bi and Wx-mq parent Kitaake (He et al. 2005). Ding et al. (2007b) studied
were simultaneously transferred into high-yielding rice the photosynthetic characteristics of sorghum C4-type
varieties, and a new rice line (Ning 9108) with improved PEPC transgenic rice and found that CO2 compensation
quality, disease resistance, yield, and agronomic traits was point and photorespiration rate significantly decreased
screened out and bred by a combination of field breeding, while light-saturated photosynthetic rate and carboxylation
resistance identification, and grain endosperm appearance rate increased in transgenic plants, reflecting the photo-
identification (Yao et al. 2010). Wang et al. (2009a) firstly synthetic characteristics of C4 plants. Wang et al. (2004a)
designed InDel markers in the coding region of ALK and also indicated that the major economic traits of PEPC
fgr, which controlled gelatinization temperature (GT) and transgenic rice, including effective panicles per plant, total
dominated the trait of rice fragrance; these two genes were grains per panicle, thousand-grain weight, and yield per
successfully introgressed in Minghui 63 lines according to plant, were respectively improved by 14.9, 5.7, 1.3, and
the progress of backcross pyramiding using the two 13.9 % compared to those of the original parent Kitaake.
developed molecular markers; the improved Minghui 63 Regarding the same traits of PEPC ? PPDK transgenic
lines exhibited significant low GT and high gel consistency rice, the effective panicles and yield per plant were,
(GC), while the white core chalkiness decreased and fra- respectively, improved by 29.1 and 27.0 % compared to
grant trait expressed in these lines; the results elucidated the receptor parent Kitaake (He et al. 2005). In BC1F1,
that the quality of Minghui63 has been improved signifi- BC2F1, and BC1F2 of PEPC-containing Shuhui 881, the
cantly in terms of rice appearance, cooking, and eating numbers of tillers, effective tillers, thousand-grain weight,
quality. and regenerated shoots all increased compared to those of
the control variety Shuhui 881. The above studies have laid
a foundation for molecular breeding of high-photosynthetic
Molecular breeding for improved physiological traits efficiency in super rice. In addition, researchers from the
National Hybrid Rice Engineering Technology Research
High-photosynthetic efficiency is one of the most physio- Center (Changsha City, Hunan Province) have mapped
logical traits for enhancing rice biomass and grain yield multiple high-yield, high-photosynthetic efficiency genes

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(Table 4), identified dozens of functional molecular genetics, physiology and biochemistry, and biological sta-
markers and candidate genes, and created a large amount of tistics in the crop breeding process. According to the
germplasms with high-photosynthetic efficiency and the breeding objectives and growth environment of specific
genes of key photosynthetic enzyme in C4 plants. crop, MDB designs the optimal scheme and then carries out
In China, rice heterosis is mainly utilized by cultivating trials of crop breeding.
male sterile line, male sterile maintainer line, and male MDB mainly involves three steps (Xu and Zhu 2012):
sterile restorer line (collectively referred to as three-line), (1) to map QTLs for all relevant agronomic traits; (2) to
so as to select dominant combinations (Sun et al. 2012). In evaluate allelic variation in these QTLs; and (3) to carry
recent years, restorer genes and wide compatibility genes out design breeding (Fig. 1). MDB generally has the fol-
have been successively cloned along with rapid develop- lowing requirements: (a) high-density molecular genetic
ment of biotechnology (Table 4), and the heterosis in map and high-efficiency molecular marker techniques;
indica and japonica subspecies has been gradually shifted (b) sufficient understanding of important genes (QTLs)
from exploratory research to practical application. regarding the location and function; (c) a complete genetic
The wide compatibility gene S5 of rice was cloned in information database established for MDB; (d) a collection
2008 (Yang et al. 2012) and rapidly used in production of germplasm and intermediate materials applicable for
practices thereafter. By designing molecular markers of S5, design breeding, including important core germplasm or
Yang et al. (2009a) have screened out two restorer lines the backbone parents and their derived RILs with target
and a large amount of new rice germplasms carrying the traits, near-isogenic lines, DH population, chromosome
wide compatibility gene S5-n. The functional markers of fragment introgression/substitution lines; and (e) improved
S5-n were useful to identify rice resources and detect statistical analysis method and relevant software developed
hybrid purity (Zhang et al. 2010a). for simulation studies on directed creation of new crop
varieties. The above conditions have been met in the case
of rice.
Prospects The development of rice breeding from conventional
genetics to molecular design of new varieties is a general
In recent years, great progress has been made on molecular trend, which ensures the breeding of new varieties with
breeding in rice and the per unit area yield of this crop has improved agronomic traits in terms of the yield, grain
been significantly improved in China. What then is the best quality, select efficiency, disease and pest resistance, and
path to increasing grain yield and further improve the stress tolerance, further contributing to the protection of
quality of rice? national food and environmental security.
First is to pay more attention to the development and
utilization of wild rice. Narrow genetic background of Open Access This article is distributed under the terms of the
Creative Commons Attribution License which permits any use, dis-
parent materials is the main cause for the undesirable crop tribution, and reproduction in any medium, provided the original
yield, quality, and resistance, while wild rice provides rich author(s) and the source are credited.
genetic resources with good traits such as strong pest
resistance and stress tolerance. Second is to understand the
vital role of wide compatibility resources in rice heterosis. References
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