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Grain pro-duction is largely influenced by the yield potential of rice varieties.. Therefore, improvement in the yield potential of rice is the major strat-egy to increase world rice p

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Strategies for increasing the yield potential of cereals: case of rice as an example

GU R D E V S KH U S H

University of California, 39399 Black Hawk Place, Davis, CA 95616-7008, USA; Corresponding author, E-mail: gurdev@khush.org

Received April 30, 2012/Accepted May 30, 2012

Communicated by P Gupta

Abstract

Rice is the most important food crop Worldwide, more than 3.5 billion

people depend upon rice for more than 20% of their calories Global rice

demand is estimated to rise from 676 million tons in 2010 to 763 million

tons in 2020 and to further increase to 852 million tons in 2035 This is

an overall increase of 176 million tons in the next 25 years To meet this

challenge rice production on existing land must be increased Grain

pro-duction is largely influenced by the yield potential of rice varieties.

Therefore, improvement in the yield potential of rice is the major

strat-egy to increase world rice production Various strategies to increase the

yield potential include; (1) conventional hybridization and selection, (2)

ideotype breeding, (3) hybrid breeding, (4) exploitation of wild species

germplasm, (5) enhancement of photosynthesis, (6) genomic approaches

and (7) physiological approaches Rice has become a model plant for

genetics and breeding research Advances in molecular biology and

genomics, proteomics and metabolics have opened new avenues to apply

innovative approaches to rice breeding Molecular-assisted selection

(MAS) has become an integral component of germplasm improvement.

A large number of genes/QTLs for various traits have been tagged with

molecular markers to apply MAS for trait improvement Genome

sequence data have become an important source for detecting allelic

var-iation It is now possible to precisely understand the role of epigenetic

changes in gene expression, thus understanding the stability of various

stresses under changing environments All these advances when

inte-grated with conventional breeding will result in designer rice varieties to

meet the challenges of rice food security in 21th century.

Key words:yield potential — rice breeding — strategies

Rice is the most important food crop and staple food of more than

half of the world’s population Worldwide, more than 3.5 billion

people depend upon rice for more than 20% of their daily calories In

most of the developing world, rice availability is equated with food

security and closely connected to political stability Rice yield

growth has fallen from 2.3% per year during 1970–1990 to 1.5%

dur-ing 1990s and to<1.0% during the first decade of present century

Global rice demand is estimated to rise from 676 million tons

in 2010 to 763 million tons in 2020 and to further increase to

852 million tons in 2035 This is an overall increase of 26% or

176 million tons in the next 25 years However, area planted to

rice in major production countries has been decreasing because

of conversion of land for housing, industries and highways

Hence, increasing rice yields on existing land remains primary

strategy for increasing production Grain production is largely

influenced by the yield potential of rice varieties Therefore,

improvement in the yield potential of rice is the major strategy

to increase world rice production To produce 176 million tons

additional paddy rice by 2035, we need to increase the yield

potential of rice from 10 to 12.3 tons per hectare

Various strategies to increase the yield potential of rice are discussed below

Conventional Hybridization and Selection

Traditional hybridization and selection is still a widely used strategy for developing crop varieties with a higher yield potential In this methodology, the segregating populations derived from crosses between two parents are screened for desirable recombinants and selected lines are evaluated in replicated yield trials This approach is therefore based on the variability created through hybridization between diverse parents and subsequent selection of desirable individuals Based on this strategy, about 1.0% increase has occurred per year in the yield potential of various cereals such as wheat, barley and rice (Peng

et al 2000) This is the time-tested strategy It is basic to all other crop improvement strategies

Ideotype Breeding (New Plant Type)

Ideotype breeding aimed at modifying the plant architecture is also time-tested strategy to increase the yield potential Thus, selection for short-statured cereals such as rice, wheat and sor-ghum resulted in doubling of their yield potential Yield is a function of total biomass and harvest index (HI) Tall and tradi-tional rice varieties could produce a biomass of 13–14 tons per hectares under most conditions, and their HI is 0.3 Their biomass cannot be increased by application of nitrogenous fertilizers as plants grow excessively tall, lodge badly and their yield decreases instead of increasing To increase the yield potential of tropical rice, it was necessary to improve biomass production and HI by increasing their nitrogen responsiveness and lodging resistance and better partitioning of photosynthates As is well known, this was accomplished by reducing plant height through incorporation

of recessive gene sd1 for short stature First semi-dwarf or short-statured variety IR8 developed at International Rice Research Institute (IRRI) also had a combination of other desirable traits such as profuse tillering, dark green and erect leaves for good canopy architecture and sturdy stems for lodging resistance It is responsive to nitrogenous fertilizer and can produce higher bio-mass of about 20 tons per hectare It has HI of 0.45 Its yield potential is 8–9 tons per hectare (Chandler 1969) This plant type was accepted widely, and most of the rice breeding programmes world over adopted this plant type To increase the yield potential

of semi-dwarf rices, further IRRI scientists proposed a new plant type (NPT; IRRI 1989) with following characteristics:

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1 Reduced tillering (9–10 for transplanted conditions)

2 No unproductive tillers

3 200–250 grains per panicle

4 Dark green and erect leaves

5 Vigorous and deep root system

6 Growth duration of 110–130 days

7 Multiple disease and insect resistance

8 Higher harvest index

Breeding efforts to develop NPT were initiated in early 1990s

Tropical japonica (TJ) varieties called bulus from Indonesia are

known to have low tillering ability, large panicles, sturdy stems

and deep root system Many bulu varieties were crossed with a

semi-dwarf japonica breeding line Sheng Nung 89–366 from

Shenyang Agricultural University, China More than 2000

crosses were made, and over 100 000 pedigree lines were

evalu-ated Breeding lines with desirable ideotype traits were selected,

and more than 500 so-called NPT-TJ lines were evaluated in

yield trials These lines had improved sink size, improved

lodging resistance and no unproductive tillers Grain yield of

these lines, however, was even lower than elite varieties It was

observed that reduced tillering contributed to lower biomass and

lower compensation ability Moreover, these NPT-TJ lines had

very poor grain filling Poor grain filling was attributed to lack

of apical dominance within a panicle, compact arrangement of

spikelets and limited number of large vascular bundles for

assimilate transport to grains Moreover, these NPT-TJ lines

were susceptible to diseases and insects and their grain quality

was not acceptable for consumers in tropical and subtropical

countries These lines were evaluated in several countries Some

of these lines showed good performance in temperate areas

where japonica grain quality is preferred Three of these lines

were released as varieties in Yunnan province of China as

Diancho 1, 2 and 3 (Khush 1995)

To improve the acceptability of these NPT-TJ lines for

tropi-cal conditions and to improve their yield potential, they were

crossed with elite indica lines and varieties with disease and

insect resistance and good grain quality More than 400 lines

designated as NPT-IJ were evaluated in yield trials Several of

these lines out yielded the best improved indica varieties such as

IR 72 by as much as 1.0–1.5 tons per hectare These breeding

lines have been continuously used in the breeding programme

and have contributed to increased genetic diversity through

introduction of japonica germplasm into otherwise indica

breeding materials Before the NPT project, japonica gene pool

was essentially excluded from the breeding programmes in

tropics Four NPT-IJ lines have been released as varieties in the

Philippines and Indonesia Numerous NPT-IJ lines were

distributed to all the breeding programmes throughout the world

through INGER nurseries Many have been used in hybridization

programmes and have contributed to widening of gene pools

For example, IR 66154- 521- 2 -2 a NPT-TJ line has been used

widely in hybridization programmes in China and Vietnam

Stimulated by IRRI’s NPT breeding programme, China

established nationwide mega project on development of super

rice Many super rice breeding lines have been developed by

Chinese breeders, which have been used as parents in hybrid rice

breeding (Peng et al 2008)

Hybrid Breeding

Hybrid breeding exploits the increased vigour or heterosis of F1

hybrids that is generally observed in outcrossing species In

maize, major yield improvement has been associated with the introduction of F1 hybrids on commercial scale, so much so all the maize area in USA and Europe is planted to hybrids Aver-age yield advantAver-age of hybrids vs varieties is approximately 15– 20% (Tollenaar 1994) Rice hybrids were introduced in China during mid-1970s and are now planted to about 13–14 million hectares or 50% of the rice area in that country The average yield advantage of hybrids over varieties is about 10–15% Rice hybrids adapted to tropical conditions have been developed

at IRRI (Virmani 2003) and by the national programmes of most

of the countries in tropical Asia but have met with limited success

At present, only about 2 million hectares are planted to hybrid rice outside of China Main reason for lack of success of hybrids on large-scale adoption is limited yield advantage of hybrids over varieties Most of the breeding programmes in tropics have utilized the indica germplasm in hybrid development, which has limited genetic diversity However, magnitude of heterosis is related to genetic diversity In their super hybrid breeding programme, Chinese scientists have developed parental lines with variable amount of japonica alleles in otherwise indica background These hybrids have better heterosis In this context, use of NPT-IJ lines

in the breeding programme for hybrid development should help improve the heterosis In the United States, two-line hybrids have been produced using temperature-sensitive male sterile lines Male sterile female lines are tropical japonicas and restorers are indicas These hybrids are reported to have as much as 25% yield advantage over varieties

Chinese Scientists under the leadership of Professor Yuan Long Peng initiated super hybrid rice breeding programme for improving the level of heterosis Like the NPT breeding programme, they proposed the following ideotype (Yuan 2001)

1 Moderate tillering capacity

2 Heavy (5 g/panicle) and drooping panicles at maturity

3 Plant height slightly taller (about 100 cm)

4 Top three leaves with following characteristics:

• Flag leaf length about 50 and 55 cm for the second and third leaves All three leaves should be above panicle height

• Should remain erect until maturity Leaf angles of flag, 2nd and 3rd leaves should be 5, 10 and 20°, respectively

• Should be narrow and V shaped (2 cm when flattened)

• Should be thick and dark green

• Leaf area index (LAI) of top three leaves should be about 6.0

5 HI of 0.55 Many hybrids of this ideotype have been developed by Chinese breeders

Exploiting the Wild Species Germplasm

Crop gene pools can be widened through hybridization of crop varieties with wild species, weedy races as well as intra-subspe-cific crosses Such gene pools can be exploited for improving many traits including yield For example, Lawrence and Frey at the Iowa State University reported that a quarter of BC2-BC4 segregants between cultivated Avena sativa and wild Avena sterilis crosses were significantly higher in grain yield than the cultivated recurrent parent Nine lines in this study when tested over years and sites had agronomic traits similar to the recurrent parent and 10–29% higher grain yield (Lawerence and Frey

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1976) Xiao et al (1996) reported that some backcross

derivatives from a cross between an Oryza rufipogon accession

from Malaysia and cultivated rice out yielded the recurrent parent

by as much as 18% They identified two QTL from wild species,

which contributed to yield increase NERICA rices developed at

WARDA through interspecific hybridization between tropical

japonica variety ‘Morobrekan’ and an accession of Oryza

glab-errima have higher yield and wide adaption to African

environ-ment Dr Brar and his colleagues at IRRI have developed

numerous breeding lines with improved yield potential from

crosses between elite breeding lines and wild species of Oryza

Enhancing Photosynthesis

In several crop species, incorporation of ‘stay green’ trait or

slower leaf senescence has been a major achievement of

breed-ers In some genotypes with slower senescence, the Rubisco

deg-radation is slower, which results in longer duration of canopy

photosynthesis and higher yields The onset of senescence is

controlled by complement of external and internal factors Plant

hormones such as ethylene and abscisic acid promote

senescence, while cytokinins are senescence antagonists

Therefore, over production of cytokinins can delay senescence

The ipt gene from Agrobacterium tumefaciens encoding

isopentenyl transferase was fused with senescence-specific

pro-moter SAG12 and introduced into tobacco plants The leaf and

floral senescence in the transgenic plants was markedly delayed;

biomass and seed yield were increased, but other aspects of plant

growth and development were normal (Gan and Amasino 1995)

This approach appears to have great potential in improving crop

yields through slowing the senescence and rubsico degradation

and thus improving the canopy photosynthesis

C4 plants such as maize and sorghum are more productive as

compared to C3 rice and wheat C4 plants are 30–35% more

efficient in photosynthesis Professor Matsuoka and colleagues at

Nagoya University initiated a project to explore the possibility of

transferring C4 enzymes from maize to rice Four enzymes are

known to be responsible for C4 photosynthetic pathway in

maize Molecular engineering strategies have been employed to

introduce some of the genes for these enzymes in rice For

example, overexpression of maize PEPC gene in rice has

pro-duced two- to threefold higher activity of this enzyme than that

in maize and the enzyme itself accounted for up to 12% of the

leaf-soluble protein (Matsuoka et al 2001) These results suggest

a possible strategy for introducing the key biochemical

compo-nents of C4 pathway of photosynthesis into C3 rice However,

all C4 domesticated plants have‘Kranz’ anatomy, and to achieve

the goal of converting C3 rice with C4 photosynthetic pathway,

it may be necessary to alter its leaf anatomy Rice germplasm

has been screened to identify some of the components of maize

anatomy For example, maize leaves have narrower vein spacing,

whereas rice has wider vein spacing Wild rice relative Oryza

barthii and Oryza australiensis have narrower vein spacing

IRRI has undertaken a collaborative project involving several

laboratories in Europe and USA funded by Bill and Malinda

Gates Foundation to explore possibility of altering the

photosyn-thetic pathway of rice If successful, there will be major

improvement in the yield potential of rice

Genomic Approaches

Completion of rice genomic sequence has facilitated the

identification and cloning of genes and QTL for yield traits

These genes/QTL can be pyramided in elite varieties to increase their yield potential through molecular marker-assisted selection (Xing and Yang 2010) Rice yield is determined by source and sink size Three grain yield components, for example number of panicles per unit area, number of spikelet per panicle and grain weight determine the sink size Genomic approaches have allowed the identification and cloning of genes for these sink traits (Sakamoto and Matsuoks 2008) These are FC1 and htd1 for tillering, Gn1a and OsSPL14 for panicle architecture, and GS3, GW2 and tgw6 for grain weight (Ashikari and Matsuoka 2006) Development, identification and validation of functional SNP markers for target genes will facilitate the pyramiding of these genes into elite germplasm through molecular marker-assisted selection Yield QTLs are derived from natural variation The use of wide range of germplasm such as wild species can

be exploited to identify genes for yield components For example, 334 introgression lines (INL) derived from crosses between IR64 and 10 donor parents were developed through backcrossing by Dr Kobayashi at IRRI Variations in agronomic characters were characterized, and introgressed segments were determined by SSR markers in each INL Fifty-four regions associated with agronomic traits such as days to heading, culm length, panicle number per plant and grain weight in the genetic background of elite variety IR64 were identified These materials are highly useful for enhancing rice yield potential

Physiological Approaches

Physiological approaches should aim at improving the radiation-use efficiency by improving the performance and regulation of Rubisco, introduction of C4-like traits such as CO2concentrating mechanisms, improvement of light interception and improvement

of photosynthesis at the whole-canopy level Efforts must focus

on identification and utilization of photosynthetically efficient germplasm Genes/QTL for efficient mobilization and loading of photosynthates from source to sink should be identified (Zhong

et al 2000) High throughput protocols for selection of more efficient germplasm in the breeding programme are needed

Prospects

Rice has become a model plant for genetic and breeding research Advances in molecular biology and genomics, proteomics, transcriptomics and metabolics have opened new avenues to apply innovative approaches to rice breeding Molecular-assisted selection (MAS) has become integral component of germplasm improvement A large number of genes/QTLs for various traits have been tagged with molecular markers to apply MAS for trait improvement Map-based cloning has resulted in isolation of several genes for resistance to biotic and abiotic stresses as well as yield-related traits These include tiller number, number of grains per panicle, grain weight and grain filling This has opened the possibility of applying MAS for yield enhancement Genome sequence data have become important resource for detecting allelic variation and genome-assisted breeding programmes Recombinant DNA technology has resulted in production of transgenic rices with new genetic traits and for resistance to biotic and abiotic stresses High throughput transformation protocols for rice, activation tagging and insertional mutagenesis have bearing for enhancing transformation efficiency RNA interference (RNAi) a sequence-specific gene-silencing technology holds promise to modify gene expression for producing germplasm resistant to diseases, insects,

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nematodes including desired modification in starch and oil

properties It is now possible to precisely understand the role of

epigenetic changes in gene expression, thus understanding the

stability of various stresses under changing environments All

these advances when integrated with conventional breeding will

result in designer rice varieties to meet the challenges of food

security in the 21st century

References

Ashikari, M., and M Matsuoka, 2006: Identification, isolation and

pyramiding of quantitative trait loci for rice breeding Trends Plant

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Chandler, R F Jr, 1969: Plant morphology and stand geometry in

relation to nitrogen In: J D Eastin, F A Haskin, C Y Sullivan, and

C H M Van Baul (eds), Physiological Aspects of Crop Yield, 265 —

285 ASA Publication, Madison, Wisconsin.

Gan, S., and R A Amasino, 1995: Inhibition of leaf senescence by

auto-regulated production of cytokinin Science 270, 1986 —1988.

International Rice Research Institute (IRRI), 1989: IRRI Towards 2000

and Beyond International Rice Research Institute, Los Banos, Laguna,

Philippines.

Khush, G S., 1995: Breaking the yield barrier of rice GeoJournal 35,

329 —332.

Lawerence, P L., and K J Frey, 1976: Backcross variability for grain

yield in species crosses (Avena sativa L 9 A sterilis L.) Euphytica

24, 77—85.

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level expression of C4 photosynthetic genes in transgenic rice In: G.

S Khush, D S Brar, and B Hardy (eds), Rice Genetics IV, 439 —

447 International Rice Research Institute, Los Banos, Laguna, Philippines.

Peng, S., R C Laza, R M Visperas, A L Sanico, K G Cassman, and

G S Khush, 2000: Grain yield of rice cultivars and lines developed in the Philippines since 1966 Crop Sci 40, 307 —314.

Peng, S B., G S Khush, P Virk, Q Tang, and Y Zou, 2008: Progress

in ideotype breeding to increase rice yield potential Field Crops Res.

108, 32 —38.

Sakamoto, T., and M Matsuoks, 2008: Identifying and exploiting grain yield genes in rice Curr Opin Plant Biol 11, 209 —214.

Tollenaar, M., 1994: Yield potential of maize: impact of stress tolerance In: K G Cassman (ed.), Breaking the Yield Barrier Proceedings of a workshop on rice yield potential in favorable environments, 103—109 International Rice Research Institute, Los Banos, Laguna, Manila, Philippines.

Virmani, S S., 2003: Advances in hybrid rice research and development

in the tropics In: S S Virmani, C X Mas, and B Hardy (eds), Hybrid Rice for Food Security, Poverty Alleviation, and Environmen-tal Protection Proceeding of the 4th International Symposium on hybrid rice, May 2002, 14 —17, Hanoi, Vietnam.

Xiao, J., S Grandillo, S N Ahn, S R McCouch, and S D Tanksley, 1996: Genes from wild rice improve yield Nature 384, 1223 —1224 Xing, Y., and Q Yang, 2010: Genetic and molecular bases of rice yield Annu Rev Plant Biol 61, 421 —442.

Yuan, L., 2001: Breeding of super hybrid rice In: S Peng, and B Hardy (eds), Rice Research for Food Security and Poverty Alleviation, 143 —

149 International Rice Research Institute, Los Banos, Philippines Zhong, S., C Lu, L Zhao, L Wang, C Q Dai, and J Zou, 2000: Physiological basis of high yield of an intersubspecific hybrid rice, liangyoupeijiu J Nanjing Agric Tech College 16, 8 —12.

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