Chapter 7

Progress and Perspectives of Distant Heterosis

in Rice

Deming Jin and Tondi Yacouba Nassirou

Abstract Heterosis, or hybrid vigor, represents one of the greatest contributions of

genetics to the improvement of major crops such as maize and rice, which is inten-
sively studied and exploited by breeders and seed companies worldwide. The
exploitation of distant heterosis is a promising way to further raise the yield poten-
tial of crops. This review describes aspects of the genetic basis for heterosis, diver-
sification of rice and its related species, principles and methodologies for exploiting
distant heterosis in hybrid rice breeding. Both promises and constraints are discussed
for understanding the importance and difficulties of distant heterosis utilization.
Progress of distant heterosis is demonstrated by the intersubspecific heterosis
between two subspecies of Asian rice (Oryza sativa L.), ssp. indica and ssp. japon-
ica, and the interspecific heterosis between two cultivated species, Asian rice and
African rice (O. glaberrima Steud.). Strategies of using the doubled haploid method
and molecular genetics approaches are suggested for accelerating distant heterosis
breeding, eliminating sterility loci to overcome the hybrid sterility of distant crosses,
and identifying and pyramiding QTLs of distant heterotic loci and favorable genes
to develop a more typical intersubspecific hybrid rice with higher ratio of indica/
japonica heterozygotic loci, and to create a more adaptive and productive partial
interspecific hybrid rice incorporating sativa/glaberrima heterozygotic loci and
favorable genes from the two cultivated species.

Keywords Doubled haploid • Genetic diversity • Heterosis breeding • Heterotic

loci • Hybrid rice • Interspecific heterosis • Intersubspecific heterosis • Oryza sativa
• Oryza glaberrima • QTL

D. Jin (*) • T.Y. Nassirou

MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of
the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural
University, Wuhan, China
e-mail: [email protected]; [email protected]

© Springer International Publishing Switzerland 2015 193

J.M. Al-Khayri et al. (eds.), Advances in Plant Breeding Strategies: Breeding,
Biotechnology and Molecular Tools, DOI 10.1007/978-3-319-22521-0_7
194 D. Jin and T.Y. Nassirou

7.1 Introduction

Hybrid vigor is widespread in plants and animals, and this phenomenon has been
observed and utilized purposely or unconsciously ever since the domestication of
crops and animals. Plant hybrid vigor was first reported by Kölreuter (1761) who
emphasized two aspects of the phenomenon, that hybrid vigor was related to the
dissimilarity of parents and that nature favored outcrossing. Darwin (1876) showed
that cross-pollination was generally beneficial while self-pollination was disadvan-
tageous in plant evolution.
Crop heterosis breeding started with cross-pollinated maize. Shull (1908) estab-
lished the concept of heterosis from his study of a maize field, discovering inbreed-
ing depression and hybrid vigor in crosses between inbred lines. He also designed a
procedure to obtain maize single hybrids. However, seed production cost of single
hybrids was too high for commercial production at the time. Jones (1918) designed
the procedure of producing double hybrids from two single hybrids to lower seed
costs, which made possible the successful commercial production of first-generation
hybrid maize. Relatively easy mechanical or hand emasculation for this diclinous
crop facilitated the early success of hybrid maize production.
Heterosis in rice was first reported by Jones (1926) who observed marked
increase in tiller number and grain yield in some F1 hybrids in comparison to their
parents. Since then, hybrid vigor has been reported for various agronomic traits
such as yield, grain weight, spikelets per panicle, panicles per plant, plant height,
days to flower, etc. (Cheng et al. 2007; Jaikishan et al. 2010; Jones et al. 1998;
Virmani 1994; Virmani et al. 1981). However, hybrid seed production via artificial
emasculation for this self-pollinated monoclinous crop was much more difficult
than that of the diclinous maize. Therefore, genetic tools such as cytoplasmic male
sterility (CMS) were essential for developing commercially hybrid rice.
Katsuo and Mizushima (1958) reported the first attempt to develop CMS rice.
The first complete CMS system derived from an intersubspecific cross between an
indica cv. Chinsurah Boro II and a japonica cv. Taichung 65 was developed in 1966.
This japonica CMS line is gametophytic male sterile. The F1 hybrid has 50 % fer-
tile pollen but almost normal fertile seed setting (Shinjyo 1975). The first japonica
hybrid rice, however, showed limited heterosis because its two parental lines were
derived from the same original cross and thus had limited genetic diversity.
The first successful commercial hybrid rice, released in China in 1973, was an
indica hybrid variety Nanyou 2. Its CMS line was derived from an interspecific
cross between a pollen abortive common wild rice plant and a Chinese local variety
Erjiu Nan and its restorer IR24 was released by IRRI (Yuan 2002). Hybrid rice cur-
rently occupies more than 16 million ha, making up more than 50 % of total rice
area in China (Li et al. 2007), and it is also being planted commercially in several
South and Southeast Asian countries (Sheeba et al. 2009). Hybrid rice produced via
both a three-line system based on CMS and a two-line system dependent on photo-
period and/or temperature-sensitive genetic male sterility (Jin et al. 1987) is culti-
vated in China, although the three-line system is still the major method for hybrid
7 Progress and Perspectives of Distant Heterosis in Rice 195

seed production in other countries. Large-scale production of hybrid rice worldwide

is still mainly confined to indica rice which shows relatively wider genetic diversity
in comparison to japonica rice.
The magnitude of heterosis of a hybrid mainly depends on the genetic diversity
between its parents. Therefore, exploiting heterosis of distant crosses is a promising
way for further raising yield potential of crops. Attempts at exploiting distant het-
erosis have been made in rice heterosis breeding; encouraging progress has been
achieved in both intersubspecific heterosis between two subspecies of Asian rice or
common rice (Oryza sativa L.), ssp. indica and ssp. japonica, and interspecific het-
erosis between two cultivated species, Asian rice and African rice (O. glaberrima
Steud.). This chapter covers aspects of the genetic basis for heterosis, diversification
of rice and its related species, potential and constraints of distant heterosis utiliza-
tion in rice, principles and methodologies for hybrid rice breeding to exploit distant
heterosis, and strategies for more effective approach to distant heterosis using dou-
bled haploid and molecular technologies to solve key problems such as hybrid ste-
rility as well as pyramiding QTLs of heterotic loci and other favorable genes.

7.2 Heterosis and Genetic Diversity

Heterosis, or hybrid vigor, refers to the phenomenon that a hybrid organism often
exhibits increased size, growth rate and productivity over those of its parents. The
fundamental ideas of heterosis (Shull 1908) include: (1) deleterious recessive alleles
persist in large random mating populations; (2) inbreeding reduces vigor due to
increasing homozygosity of deleterious alleles and (3) vigor is restored by crossing
divergent inbred lines as recessive deleterious alleles are complemented in the
hybrid. Crop breeders exploit heterosis by mating two divergent inbred lines that
have complementary desirable traits. The F1 hybrids generally show heterosis with
desired characteristics of both parents.
Classical genetic theories of heterosis are divided into three categories: domi-
nance hypothesis (Bruce 1910; Davenport 1908): overdominance hypothesis (Crow
1948; Hull 1945) and epistatic hypothesis (Powers 1944; Williams 1959). The dom-
inance hypothesis suggests the complementary effects between different desirable
dominant alleles from the two parents result in the superiority of hybrids, whereas
the overdominance hypothesis focuses on the strong interaction effects between dif-
ferent allelic genes from the parents. The epistatic hypothesis, however, emphasizes
the role of non-allelic gene interactions in hybrids. These three classical hypotheses
of heterosis have been analyzed by new molecular technologies such as molecular
markers and QTL mapping. Molecular evidences supporting the three hypotheses
respectively have been found by different researchers (Fu et al. 2014; Hua et al.
2003; Larièpe et al. 2012; Melchinger et al. 2007; Piepho 2009; Schön et al. 2010;
Schrag et al. 2009).
Emerging genomic and epigenetic studies have provided new insights into the
genetic basis of heterosis (Chen 2013; Groszmann et al. 2013). Heterosis may arise
196 D. Jin and T.Y. Nassirou

from allelic and non-allelic interactions between parental genomes, thus changing
the programming of genes that promote the growth, development, stress tolerance
and fitness of hybrids. Epigenetic modifications of key regulatory genes in hybrids
can alter complex regulatory networks of physiology and metabolism, leading to the
expression of heterosis in complex traits such as grain yield.
Genetic diversity between parents is the primary cause of heterosis in the hybrid.
Breeders have extensively investigated the genetic diversity between parents and its
relationship with heterosis of the hybrid for predicting heterotic cross combinations.
Most researchers found positive correlations between the genetic diversity and het-
erosis, i.e. the greater the genetic distances between two parents, the higher the
possibility to obtain hybrids with strong heterosis. For example, genetic distances
analysis revealed by both traditional methods based on agronomic-morphological
traits and molecular markers were positively correlated with heterosis in maize
(Larièpe et al. 2012) and rice (Kaw 1995; Luo et al. 1996, 1999; Mahapatra et al.
1995; Phetmanyseng et al. 2010; Saghai et al. 1997; Xu et al. 2002). However, the
correlation between the genetic distance and heterosis depends on the materials and
traits investigated (Zhou et al. 2012).
Although genetic diversity between parents is often emphasized to be positively
correlated to heterosis of hybrids, it is also correlated to hybrid sterility (Moehring
2011). Reproductive isolation can occur when the genetic distance between parents
surpasses a critical point. Negative heterosis of traits related to sexual reproduction
such as seed set rate and grain yield may happen when crossing two distantly related
parents. Reduced vigor or outbreeding depression is sometimes observed in distant
crosses. For example, the hybrid sterility problem remains a crucial factor that nega-
tively affects grain yield in distant crosses of rice, resulting in low seed set rate in
intersubspecific crosses between indica and japonica rice (Li et al. 1997; Long et al.
2008), and almost zero seed setting in interspecific crosses between Asian and
African rice (Adedze et al. 2012; Heuer and Miezan 2003; Koide et al. 2008; Sano
1986).

7.3 The Diversification of Rice

The genus Oryza has 23 species with 10 recognized genome types (AA, BB, CC,
BBCC, CCDD, EE, FF, GG, HHJJ and HHKK), including 21 wild species and 2
domesticated species (Gramene.org). The two cultivated species, Asian rice (O.
sativa) and African rice (O. glaberrima), both have the AA genome but they were
independently domesticated from different progenitors of wild species in different
geographic locations, respectively (Fig. 7.1).
The Asian rice was domesticated from the Asian common wild rice (Oryza rufi-
pogon) approximately 10,000 years ago in Southern Asia and most probably in
southern China (Jiang and Liu 2006; Molina et al. 2011; Sweeney and McCouch
2007). Asian rice contains two major subspecies: ssp. indica and ssp. japonica. The
indica rice is grown throughout tropical and subtropical Asia. The japonica rice,
7 Progress and Perspectives of Distant Heterosis in Rice 197

Gondwanaland

Common ancestor
Oryza AA genome species

Southern Western
Asia Africa

Wild perennial O. rufipogon (AA) O. longistamimata (AlAl)

species

Wild annual O. nivara (AA) O. barthii (AgAg)

species

Cultivated O. sativa (AA) O. glaberrima

species (AgAg)
ssp. indica ssp. japonica

Fig. 7.1 The evolution and domestication of two cultivated rice species

which is more tolerant to low temperatures, is mainly cultivated in temperate East

Asia or in high elevation areas in South and Southeast Asia. Previous archaeological
and genetic marker studies suggest that indica was domesticated from O. rufipogon
growing in the lowland regions of Southern China; japonica rice was later devel-
oped in upland regions and selected from indica rice (Oka and Morishima 1982). A
molecular study demonstrated that the japonica subspecies suffered a more severe
bottleneck than the indica subspecies and thus a greater loss of genetic variation
during its domestication, supporting the non-independent domestication of the two
rice subspecies (Gao and Innan 2008). However, some molecular evidence suggests
the two subspecies might have been domesticated from different O. rufipogon pro-
genitors (Cheng et al. 2003; Li et al. 2012; Londo and Schaal 2007; Wei et al. 2012).
Although the domestication history of Asian rice remains a controversial issue
(Ikehashi 2009), it has been introduced successfully to Europe, Africa, America and
Australia and it is now the major cultivated species worldwide.
African rice derived from the wild species Oryza barthii originated in West
Africa around 1000 BC (Agnoun et al. 2012; Linares 2002; Murray 2004; Portères
1962; Wang et al. 2014). Its productivity is much lower in comparison to Asian rice,
but it is well adapted to certain extreme environments and possesses traits resistant
or tolerant to biotic and abiotic stresses including drought, iron toxicity, virus dis-
ease and weed competitiveness etc. (Barry et al. 2007; Efisue et al. 2009a; Gutierrez
et al. 2010; Hiroko et al. 1962; Wang et al. 2014). African rice continues to be cul-
tivated sporadically in West Africa.
198 D. Jin and T.Y. Nassirou

The common ancestor AA-genome species of the two cultivated rice species
probably occurred in Gondwanaland, and their respective progenitors diverged
between one and two million years ago after the breakup of the ancient continent
(Ma and Bennetzen 2004; Vaughan et al. 2008). Recent comparative genomic anal-
yses on Asian rice and the other five diploid AA-genome species including African
rice revealed rapid diversification of AA genomes with massive levels of genomic
structural variation, including segmental duplication and gene family turnover, with
particularly high instability in defense-related genes (Zhang et al. 2014).

7.4 Promises and Constraints of Distant Heterosis in Rice

The rich genetic diversification of Asian rice and closely related AA-genome spe-
cies has provided opportunities for exploiting distant heterosis in rice. Three catego-
ries of heterosis in rice have been defined based on the genetic diversity between
parental lines:
Intra-subspecific heterosis is resulted from the interaction of different genes
from two parental varieties belonging to the same subspecies, either indica or
japonica rice.
Intersubspecific heterosis is resulted from the interaction of different genes
between the two subspecies, indica and japonica rice, respectively.
Interspecific heterosis is resulted from the interaction of different genes from two spe-
cies respectively, such as Asian rice vs. African rice, or Asian rice vs. a wild rice species.
Since the heterosis of hybrids is generally positively correlated to the genetic
diversity of the parents, the heterosis of distant crosses including intersubspecific
and interspecific crosses is theoretically higher than that of the intra-subspecific
crosses (Fig. 7.2).

O. sativa × O. glaberrima

indica × japonica
indica × indica
japonica × japonica

Fig. 7.2 Theoretic heterosis expression of intra-subspecific hybrids of japonica or indica rice
intersubspecific hybrids between indica and japonica rice and interspecific hybrids between Asian
and African rice as estimated according to their genetic diversity
7 Progress and Perspectives of Distant Heterosis in Rice 199

While the observed vegetative vigor of the hybrids of different categories of

genetic diversity generally conforms to the theoretical expectations, the actual grain
yield of distant crosses, however, is discouraging due to the low seed set rate of the
intersubspecific hybrids between indica and japonica rice and almost no seed set-
ting in the interspecific hybrids between two cultivated species. Apparently, hybrid
sterility is a major obstacle for exploiting the distant heterosis in rice.
Reproductive isolation mechanisms restrict gene exchange between diverging
species or populations include prezygotic barriers that limit the potential for mating
or zygote formation and postzygotic barriers that reduce the fertility of hybrid off-
spring, which plays a vital role during speciation in evolution (Andrea and Willis
2012). The hybrid sterility of distant crosses is a typical form of postzygotic barrier.
The Dobzhansky-Muller model (Dobzhansky 1937; Muller 1942) explains that
hybrid sterility can be caused by incompatible gene interactions between two
diverging species or populations (Fig. 7.3).
Ikehashi et al. (1984, 1986) studied hybrid sterility between indica and japonica
rice and screened for compatibility varieties to overcome the intersubspecific repro-
ductive barrier and proposed a model which is essentially consistent with the
Dobzhansky-Muller model to explain the intersubspecific hybrid incompatibility.
The two incompatibility alleles designated as S5i and S5j for indica and japonica,
respectively, and deleterious interactions between S5i and S5j resulted in reduced
spikelet fertility of the intersubspecific hybrid. They also reported an additional
allelic gene S5n, which could overcome the fertility barrier in the indica/japonica
hybrids and thus it is named a wide-compatible (WC) gene. Molecular studies have
revealed the precise location of the S5n gene on chromosome 6 (Ji et al. 2005) and

Fig. 7.3 The Dobzhansky-Muller model for a single-locus hybrid incompatibility: an ancestral
population splits into two geographically isolated populations that diverge genetically and eventu-
ally fix different alleles (red or blue) at the same locus. In the F1 hybrid, these two derived alleles
are incompatible (Source: Adopted from Andrea and Willis (2012))
200 D. Jin and T.Y. Nassirou

its genetic mechanism and complex evolution (Du et al. 2011). Further study
revealed a killer-protector system at the S5 locus encoded by three tightly linked
genes (ORF3, ORF4 and ORF5) regulates fertility in indica-japonica hybrids. The
combined actions of ORF5+ (killer) and ORF4+ (partner) cause endoplasmic reticu-
lum (ER) stress. ORF3+ (protector) prevents ER stress and produces normal gam-
etes, but ORF3− cannot prevent ER stress, resulting in premature programmed cell
death that leads to embryosac abortion (Yang et al. 2012). The discovery of wide-
compatible gene S5n greatly encouraged research on intersubspecific heterosis
utilization.
A more intensive and complex reproductive isolation including both prezygotic
and postzygotic barriers exists in the crosses between O. sativa and O. glaberrima
(Sano et al. 1986). Several major genes responsible for the interspecific hybrid ste-
rility between the two species have been detected from O. glaberrima, such as S1
(Guyot et al. 2011; Heuer et al. 2003; Koide et al. 2008), S29 (Hu et al. 2006) and
S36 (Li et al. 2011). The interspecific hybrid sterility was mainly caused by an arrest
of pollen development at the microspore stage (Bimpong et al. 2011). However, S1
could induce abortion of both male and female gametes possessing its allelic alter-
native (Koide et al. 2008). No effective wide-compatibility gene has been reported
to overcome the interspecific reproductive isolation up to present. The hybrid steril-
ity problem remains a major concern for exploiting the interspecific heterosis
between the two cultivated species (Abebrese et al. 2011; Adedze et al. 2012).

7.5 Intersubspecific Heterosis between indica and japonica

Rice

Spontaneous intersubspecific hybrid plants from open pollination between indica

and japonica rice growing in adjacent paddy fields in previous seasons are often
seen in regions growing both subspecies. They are called big green plants by rice
farmers because of their prominent features of longer growth duration, taller and
more robust stems, big panicles with fewer filled grains and usually staying green
when all other rice plants are turning yellow at maturity in the paddy field. It is
apparent that positive heterosis exists in both yield related source traits such as leaf
area and biomass, and sink traits such as spikelets per panicle. Most rice breeders
are convinced that there is strong heterosis in the intersubspecific hybrids between
indica and japonica rice (Yang and Liu 1991; Yuan et al. 1994). However, the appar-
ent negative heterosis in grain yield is caused by spikelet sterility which blocks the
photosynthetic products from the source flow into the sink.
Because the postzygotic reproductive barrier of hybrid sterility constitutes a bot-
tleneck for exploiting the intersubspecific heterosis, the genetic mechanism of
intersubspecific hybrid sterility has been extensively studied. Both embryosac abor-
tion and pollen sterility are found to be associated with the intersubspecific hybrid
sterility. Sterility gene S5 (Ikehashi and Araki 1986), S24 and S35 (Qiu et al. 2005)
7 Progress and Perspectives of Distant Heterosis in Rice 201

have been identified to cause intersubspecific hybrid sterility between indica and
japonica rice. The identification of more than one sterility gene explained why the
wide compatibility genes S5n alone could not always effectively overcome the
reproductive barrier between the two subspecies of rice.
Remarkable progress has been achieved in the intersubspecific heterosis breed-
ing in China. Chinese rice breeders have adopted a more effective approach to over-
come the reproductive barrier by producing partial intersubspecific hybrids, rather
than simply depending on the wide compatible gene. For example, testing crosses
between indica varieties and chromosome segment substitution lines (CSSL) carry-
ing japonica genes in the genetic background of indica proved to be effective for
improving yield potential of hybrid rice (Wang et al. 2012). The super rice program
sponsored by the Chinese Ministry of Agriculture has announced a few super high
yielding hybrid varieties that incorporated intersubspecific heterosis (Table 7.1),
including 4 indica-japonica hybrid varieties, i.e. Yongyou6, Yongyou12 and
Yongyou15 released by the Ningbo Academy of Agricultural Sciences, and
Chunyou84 released by the China National Rice Research Institute (Fig. 7.4c).
Hybrid varieties with a relatively small proportion of intersubspecific heterozy-
gotic loci are usually recognized as intra-subspecific hybrid varieties. For example,
a super high yielding hybrid variety Xieyou 9308 carried about 12.5 % japonica
genes as estimated according to the pedigree of its male parent Zhonghui9308,
which was derived from an intersubspecific multi-cross C57(japonica)/
No300(indica)//IR26(indica) (Cheng et al. 2007). The initial female parent C57
itself was a japonica restorer also derived from an intersubspecific multi-cross
IR8(indica)/Taida1(japonica)//Nonglin34(japonica). Xieyou 9308 was regarded as
an indica hybrid because of its relatively low japonica genomic composition.
Similarly, almost all three-line japonica hybrids contained a small fraction of indica
genomic genes because the restorer genes of their pollen parents came from indica
rice.
Recently released indica-japonica hybrids Yongyou12 and Yongyou15 have a
common restorer line F5032 derived from an intersubspecific cross carrying up to
49 % of indica genes as evaluated by molecular markers. Although the two half-
brother varieties have different female parents, a japonica CMS line Yongjing2A
and an indica CMS line JingshuangA, respectively, both are named as intersubspe-
cific indica-japonica hybrids (Liu 2012; Lu et al. 2007) because they have relatively
higher percentages of intersubspecific heterozygous loci.
The new indica-japonica hybrid rice is now very popular and has a total area of
over a million hectares in China. The hybrid variety Yongyou12 scored a record
high yield of 15,214.5 kg/ha in 2012. Still, most so-called indica-japonica hybrid
varieties released in China up to present are actually partial intersubspecific hybrids
with one of their parents derived from indica/japonica crosses (Table 7.1) instead of
a direct intersubspecific hybrids between a typical indica rice and a typical japonica
rice with wide compatibility genes to overcome its hybrid sterility, which is still the
ultimate goal.
The two subspecies of rice possess different favorable traits respectively. For
example, the indica rice generally has more tillers and is more resistant to heat
202 D. Jin and T.Y. Nassirou

Table 7.1 Hybrid rice varieties incorporated intersubspecific heterosis released in China
Subspecies/source of the parents Year
Hybrid variety Parental combination Female Male released
1
Xieyou 9308 Xieqingzao A/R9308 indica CMS indica restorer 1995
derived from
indica/japonica
2
Jinyou207 Jin23A/Xianhui207 indica CMS indica restorer 1998
derived from
indica/japonica
3
Liangyou Pei’ai 64 S/R9311 EGMS derived indica restorer 2001
Peijiu from
indica/japonica
4
Liaoyou 5218 Liao 5216A/C418 japonica CMS japonica restorer 2001
derived from
indica/japonica
5
II you 602 II-32A/Luhui 602 indica CMS indica restorer 2002
derived from
indica/japonica
6
II you 7954 II-32A/Zhehui 7954 indica CMS indica restorer 2002
derived from
indica/japonica
1
Guodao 1 Zhong 9A/R8006 indica CMS indica restorer 2004
derived from
indica/japonica
1
Guodao 3 Zhong 8A/R8006 indica CMS indica restorer 2004
derived from
indica/japonica
1
Guodao 6 Neixiang 2A/R8006 indica CMS indica restorer 2006
derived from
indica/japonica
7
Yongyou6 Yongjing2A/K4806 japonica CMS Intermediate restorer 2005
derived from
indica/japonica
7
Yongyou12 Yongjing2A/F5032 japonica CMS Intermediate restorer 2010
derived from
indica/japonica
7
Yongyou15 JingshuangA/F5032 indica CMS Intermediate restorer 2012
derived from
indica/japonica
1
Chunyou84 Chunjiang16A/C84 japonica CMS Intermediate restorer 2013
derived from
indica/japonica
Note: Hybrid varieties were released by
1. The China National Rice Research Institute
2. Hunan Hybrid Rice Research Center
3. The Academy of Agricultural Sciences of Jiangsu Province
4. The Academy of Agricultural Sciences of Liaoning Province
5. The Academy of Agricultural Sciences of Sichuan Province
6. The Academy of Agricultural Sciences of Zhejiang Province
7. The Ningbo Academy of Agricultural Sciences
7 Progress and Perspectives of Distant Heterosis in Rice 203

stress, while the japonica rice has more erect and greener leaves and is more toler-
ant to cold stress. A successful intersubspecific hybrid could have combined favor-
able traits of both species in addition to strong positive heterosis in yield related
agronomic traits (Fig. 7.4).

Fig. 7.4 The development of intersubspecific hybrid rice. (a) Panicles of indica rice at maturity.
(b) Panicles of japonica rice at maturity. (c) Field performance of a partial intersubspecific hybrid
rice (Chunyou84, released by the China National Rice Research Institute in 2013), showing an
intermediate form of panicle type between indica and japonica rice (Credit: Image courtesy of the
China National Rice Research Institute)
204 D. Jin and T.Y. Nassirou

7.6 Interspecific Heterosis Between Asian and African Rice

Written records of African rice (Oryza glaberrima) began when the first Portuguese
explorers reached the West African coast and witnessed the cultivation of rice in the
floodplains and marshes of the Upper Guinea Coast in 1446. African rice was
believed to have been domesticated and cultivated by the local inhabitants many
centuries before the first Europeans arrived and this cereal played a very important
role in the native diet. Asian rice (O. sativa) was introduced into West Africa by the
Europeans beginning in the sixteenth century, the species spread and was adopted
by local peoples who had previous experience growing the African rice species.
African rice (O. glaberrima) varieties have certain negative features in comparison
to the Asian rice (O. sativa): the seeds shatter easily, the grains are brittle and dif-
ficult to mill, and more importantly, the yields are lower. As a result, African rice O.
glaberrima has been replaced gradually by the introduced Asian rice (O. sativa) as
the major cultivated species (Agnoun et al. 2012; Linares 2002; Murray 2004).
The Oryza glaberrima varieties also offer distinct advantages: the plants have
luxurious wide leaves that shade out weeds, and the species is more resistant to
diseases and pests. In addition, African rice is more tolerant of fluctuations in water
depth, iron toxicity, infertile soils, severe climates and human neglect. Some O.
glaberrima varieties also mature faster than O. sativa varieties, making them impor-
tant as emergency food. Some African rice (O. glaberrima) varieties have survived
for one more reason: the supreme deity in ritual contexts of the traditional religion.
It was believed that the rain god gave Diola rice (O. glaberrima) to their ancestors
(Linares 2002).
African rice (O. glaberrima) is a valuable germplasm attractive to rice breeders.
It is a unique germplasm with distinct advantages as compared with the wild species
of genus Oryza. First of all, it is a cultivated species which has undergone about
3000 years of artificial selection, which conserved relatively favorable agronomic
traits. Secondly, it has a relatively appropriate genetic distance to Asian rice (O.
sativa), more distant than the AA-genome common wild rice (O. rufipogon) but
closer than many other wild species with different genome types, which make it an
ideal counterpart for exploiting interspecific heterosis. Last but not least, it pos-
sesses rich defense-related genes resistant to various abiotic and biotic stresses,
which may facilitate development of more adaptive rice. However, the intensive
reproductive isolation including both prezygotic and postzygotic barriers in the
interspecific crosses between O. sativa and O. glaberrima makes rice genetic
improvement by crossing the two species extremely difficult (Ikeda et al. 2009).
The NERICA rice varieties derived from interspecific crosses between the two
cultivated rice species via in vitro embryo rescue and anther culture techniques in
the African Rice Center (WARDA 2000, 2006; africarice.org) has provided a suc-
cessful example for developing elite inbred varieties with higher productivity and
stronger stress tolerance by combining the favorable genes of both species (Aluko
2003; Bimpong et al. 2010; Efisue et al. 2009a, b; He et al. 2010; Ikeda et al. 2009;
Ndjiondjop et al. 2012; Semagn et al. 2007). The NERICA rice has demonstrated
7 Progress and Perspectives of Distant Heterosis in Rice 205

the possibility of a favorable recombination of beneficial genes of the two cultivated

rice species to create a new type of inbred rice. Is it possible to take one more step
forward, to develop a new type of hybrid rice incorporating the interspecific hetero-
sis between the two cultivated rice?
Although almost all direct interspecific hybrids are completely sterile, it could be
possible to develop fertile partial interspecific hybrid (PIH) rice by crossing Asian
rice male sterile lines to introgression line restorers (ILR) carrying African rice
genes. Efforts have been made to develop PIH varieties with higher yield potential
in Huazhong Agricultural University since 2004 (Jin et al. 2012). New indica CMS
lines with Oryza glaberrima cytoplasm (AF-CMS) have been developed (Huang et
al. 2012). The AF-CMS lines were completely sterile whereas the fertility of its F1
hybrids was readily restored. The development of AF-CMS system has made avail-
able a third species, O. glaberrima, in addition to O. rufipogon and O. sativa, as the
cytoplasmic source of CMS for commercial hybrid rice production, which should
further help diversify the sterile cytoplasms for the three-line hybrid rice. The indica
ILRs carrying African rice genes and effective restorer genes (Table 7.2) have also
been obtained (Adedze et al. 2012). Some ILRs show certain traits which are inter-
mediate between the two cultivated species O. sativa and O. glaberrima, such as the
middle-sized sterile lemmas on the grains (Fig. 7.5b). Three-line PIHs or two-line
PIHs can be produced by crossing CMS lines or PTGMS lines to the ILRs as pollen
parents, respectively. A few PIH rice showed outstanding high yield potential
(>20 % higher than control varieties of indica hybrid, unpublished data) in field
experiments (Fig. 7.5c).
Developing introgression line restorers with an appropriate genome composition
is crucial to mitigate reproductive barrier and exploit interspecific heterosis between
Oryza glaberrima and O. sativa. A moderate introgression of O. glaberrima genes
(15–30 %) into ILRs was considered to be favorable for producing high yielding

Table 7.2 Pedigree of ILR Pedigree

introgression line restorer
ILR1 RAM3/Paddy//Paddy///Mianhui725
(ILR) carrying genes of
Oryza glaberrima ILR2 RAM152/Paddy//Paddy///Mianhui725
ILR3 RAM3/Jin23B//Jin23B///YuetaiB
ILR4 RAM3/Jin23B//Jin23B///Jin23B
ILR5 RAM3/Jin23B//Wanxian98
ILR6 RAM3/Jin23B//Nongxiang16///
Minghui63
ILR7 RAM152/Paddy//Paddy///Jiachunnian
ILR8 RAM54/Jin23B//Wanxian98///R80
ILR9 RAM3/Jin23B//Nongxiang16//
Minghui63////Basmati370
Note: RAM3, RAM54 and RAM152 are acces-
sions of African rice (O. glaberrima). All the
other varietal names are indica varieties (O.
sativa ssp. indica)
206 D. Jin and T.Y. Nassirou

Fig. 7.5 The development of partial interspecific hybrid rice. (a) Panicles of Asian rice (left),
African rice (right) and interspecific F1 (the two in middle) at maturity. The panicle of Asian rice
is much bigger than that of the African rice. And the interspecific F1 is completely sterile with long
red awns Lingshui, China 2006. (b) Grains of Asian rice (right), African rice (left) and the intro-
gression lines (ILs) (middle). African rice grain has two prominent sterile lemmas at two sides;
Asian rice grain has tiny degenerated sterile lemmas at bottom, while the size of the sterile lemmas
on the grains of some ILs falls in between the two cultivated rice. (c) Field performance of a partial
interspecific hybrid rice (AF-ST1A/ILR1) (Huazhong Agricultural University, Wuhan, China
2014). The female parental line AF-ST1A is an indica CMS line with African rice cytoplasm while
the male parent ILR1 is an indica introgression line carrying genes of African rice

PIHs. Further improvement of the genomic composition of ILs and the yield perfor-
mance of the PIHs could be achieved via marker-assisted selection for pyramiding
interspecific heterotic QTL loci and eliminating sterility genes.
7 Progress and Perspectives of Distant Heterosis in Rice 207

7.7 Strategies for More Effective Approach to Distant

Heterosis

Conventional plant breeding has dramatically increased the productivity and quality
of plants grown for food, fodder and industrial use; it has been practiced for hun-
dreds of years, and is still widely used today. The basic methods involve crossing
two different parents, followed by pedigree selection dependent on phenotyping
through generations of self-pollination, until a set of derived lines that combines the
favorable characteristics of both parents is obtained. This traditional methodology,
however, is labor intensive, time consuming and rather inefficient. It usually takes
8–10 years or more from start to finish for developing a new variety in annual crops.
This situation can be changed with the advent and dissemination of new tech-
nologies such as doubled haploid (DH) methodology and molecular genetics. For
example, conventional breeding procedures commonly take eight or nine genera-
tions to achieve approximately complete homozygosity inbred lines; more genera-
tions are needed to obtain genetically-stable inbred lines derived from distant
crosses, whereas DH lines achieve it in just one generation regardless of the types
of crosses. Precise genotyping by marker assisted selection (MAS) is much more
efficient and labor-saving than traditional visual phenotyping.
Doubled haploid (DH) lines can be produced by androgenesis or in vitro anther
culture and parthenogenesis or in vivo induction of maternal haploids. The DH lines
based on in vivo techniques have been routinely applied in commercial hybrid
maize. The major advantages of DH lines in hybrid maize breeding include the
complete homozygosity and maximum genetic variance, as well as short time to
market etc. (Geiger and Gordillo 2009). However, the DH produced by in vitro
anther culture is the more common method used in rice breeding (Alemanno and
Guiderdoni 1994; Reiffers and Freire 1990; Yi et al. 2014). Anther culture response
or androgenetic potential is largely species and genotype dependent. DH lines are
more readily induced via anther culture of Oryza glaberrima as well as O. sativa
ssp. japonica genotypes, while O. sativa ssp. indica genotypes are more recalcitrant
(Gueye and Ndir 2010; Reiffers and Freire 1990). DH plants can be produced via
spontaneous chromosome doubling of the haploid cells of the callus induced from
the microspore, while artificial chromosome doubling with colchicine treatment
effectively increases doubled haploid plant regeneration in anther culture of rice
(Alemanno and Guiderdoni 1994). Before a more effective in vivo technique is set
up, DH lines produced by anther culture can be used to accelerate distant heterosis
breeding in rice.
Molecular genetics has provided powerful tools to study the genetic basis of
heterosis and made monitoring the transmission of foreign genes into introgression
lines possible. Although we are still at the beginning of understanding the complex
mechanism of heterosis, advances of molecular genetics, especially genomics, will
facilitate the investigation and the understanding of heterotic alleles involved in
distant crosses. QTL mapping of heterotic loci of yield related traits is a particularly
important foundation work for heterosis breeding in rice (Wang et al. 2013). Fine
208 D. Jin and T.Y. Nassirou

mapping of the molecular markers closely linked to distant heterotic loci and other
favorable genes as well as sterility genes is essential for pyramiding distant heter-
otic alleles and favorable genes and eliminating the sterility genes in elite ILs to be
used as parents of hybrids incorporated distant heterosis.
The success of indica-japonica hybrid rice in China has demonstrated the poten-
tial of intersubspecific heterosis. However, these hybrids currently planted in China
are partial intersubspecific hybrids with relatively limited indica/japonica heterozy-
gotic loci. Developing more typical intersubspecific hybrids with higher ratio of
indica/japonica heterotic loci and employing more wide compatibility genes is a
promising approach to realize the full potential of the intersubspecific heterosis.
The two cultivated rice species Oryza glaberrima and O. sativa constitute a
potential genetic reservoir for breeding hybrid rice incorporated interspecific het-
erosis. However, a phenomenon known as the reproductive barrier constitutes a
bottleneck for exploiting heterosis in this more distant cross. Strategies have to be
developed to overcome or circumvent the crossing barriers and F1 hybrid sterility.
Introgression lines containing a short alien chromosome fragment could be devel-
oped. Since each introgression line has only a fragment of alien chromosome, it can
be effectively monitored to eliminate sterility genes. Technologies such as embryo
rescue, anther culture and molecular markers can be employed for more effective
approach to the interspecific heterosis between the two cultivated rice.
A pragmatic technical route is proposed for effective distant heterosis breeding.
Doubled haploid lines via anther culture are used to speed up the development of
genetically stable ILs to be used as parental lines of hybrids incorporated distant
heterosis. Marker assisted selection is used for pyramiding distant heterotic alleles
and favorable genes and eliminating the sterility genes to obtain elite ILs which are
used as pollen parents to cross with indica/japonica CMS lines or PTGMS lines to
produce experimental three line or two line hybrids incorporated distant heterosis
(Fig. 7.6).

7.8 Conclusions and Prospects

The ultimate goal of all rice breeding programs is to continuously develop varieties
with higher yield potential, superior grain quality and increased tolerance to abiotic
and biotic stresses. Exploiting distant heterosis provides a promising approach to
this goal.
Remarkable progress has been achieved in the intersubspecific heterosis breed-
ing in China. The intersubspecific indica-japonica hybrid rice has already been
grown successfully in large hectarage in China, demonstrating super high yield as
well as combined favorable traits of both subspecies.
Significant progress has also been achieved in the interspecific heterosis between
two cultivated rice. The partial interspecific sativa-glaberrima hybrid rice grown in
experimental fields shows super high-yielding potential as well as combined favor-
able traits of both species.
7 Progress and Perspectives of Distant Heterosis in Rice 209

Distant Interspecific crosses Intersubspecific crosses

crosses O. glaberrima × O. sativa O. sativa ssp. japonica × O. sativa ssp. indica

Embryo rescue

Multiple Interspecific F1 O. sativa Intersubspecific F1

× ×
crosses (Sterile) indica/japonica (Semi-sterile)

DH lines Fertile F1
production Anther culture and chromosome doubling

Doubled haploid lines

Pyramiding distant heterotic alleles and

Marker-assisted
favorable genes
selection
Eliminating the sterility genes

CMS lines Elite introgression lines P(T)GMS lines

× (restorer) ×
indica/japonica indica/japonica

Three-line hybrid rice Two-line hybrid rice

Experimental
Incorporated interspecific or Incorporated interspecific or
hybrids
intersubspecific heterosis intersubspecific heterosis

Fig. 7.6 Technical route proposed for effective distant heterosis breeding

Future prospects may be dependent on the more effective use of new technolo-
gies such as doubled haploid (DH) methodology and molecular marker technology.
For example, the employment of DH may greatly accelerate the breeding for elite
ILRs carrying foreign genes for exploiting distant heterosis. Screening and pyra-
miding intersubspecific and interspecific heterozygous loci could enhance the
understanding of the mechanisms of distant heterosis and facilitate its utilization in
hybrid rice breeding. Identification and elimination of major sterility genes could
help to overcome the hybrid sterility of distant crosses. The combination between
parents carrying more heterotic loci and exempting major sterility genes may lead
to the development of a more typical intersubspecific hybrid rice with a higher ratio
of indica-japonica heterozygotic loci and the creation of a more adaptive and pro-
ductive partial interspecific sativa-glaberrima hybrid rice.

Acknowledgements The study of interspecific heterosis was funded by the Natural Science
Foundation of China (NSFC: 30871703), the National High Technology Research and Development
Program (863 Program) of China (2012AA101101), the Natural Science Foundation of Hubei
province (2010CBB01901), and the Fundamental Research Funds for the Central Universities
(2009PY025).
210 D. Jin and T.Y. Nassirou

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