1 Introduction

The quest for increasing rice yield has been a pivotal focus in agricultural research, driven by the need to ensure global food security amidst a growing population and diminishing arable land. Hybrid rice, which leverages the phenomenon of heterosis or hybrid vigor, has emerged as a significant breakthrough in this endeavor. Heterosis refers to the superior performance of hybrid offspring compared to their parents, particularly in terms of yield and other agronomic traits (Huang et al., 2016; Gaballah et al., 2022). The integration of intersubspecific heterosis, which involves crossing different subspecies of rice, has shown promise in further enhancing the yield potential of hybrid rice varieties (Li et al., 2016; Qian et al., 2016). This study aims to explore the advancements in hybrid rice breeding by integrating intersubspecific heterosis with high-yield traits, thereby contributing to the development of superior hybrid rice varieties.

Hybrid rice has played a crucial role in addressing global food security challenges. Since its introduction, hybrid rice has significantly increased rice production, particularly in countries like China, where it has been extensively adopted (Cheng et al., 2001; Zhou et al., 2022). The ability of hybrid rice to produce higher yields compared to conventional varieties makes it a vital component in the strategy to meet the rising food demands. The exploitation of heterosis in hybrid rice has not only improved yield but also enhanced other important traits such as disease resistance and stress tolerance, further contributing to its importance in sustainable agriculture (Wu, 2009; Huang et al., 2015). The continuous improvement and adoption of hybrid rice are essential to ensure a stable and sufficient food supply for the growing global population.

Recent research has focused on understanding the genetic and molecular mechanisms underlying heterosis to optimize hybrid rice breeding. Studies have identified numerous quantitative trait loci (QTLs) and specific genes associated with yield heterosis, providing insights into the genetic architecture of hybrid vigor. The integration of intersubspecific heterosis, which involves crossing indica and japonica subspecies, has been partially exploited to develop high-yielding hybrid rice varieties. This approach has led to the identification of favorable alleles and the development of parental lines with enhanced compatibility and yield potential. Advanced genomic and transcriptomic analyses have further elucidated the complex interactions between different genetic components, paving the way for more targeted and efficient breeding strategies.

2 History and Development of Hybrid Rice

2.1 Development history of hybrid rice

The development of hybrid rice has been a significant milestone in agricultural science, particularly in the quest to meet the increasing global demand for rice. The introduction of semidwarf varieties and hybrid rice in the last century marked two major breakthroughs that significantly boosted rice productivity (Qian et al., 2016). The first successful hybrid rice variety, developed in China, demonstrated the potential of hybrid vigor or heterosis to enhance yield. This success led to the widespread adoption of hybrid rice, which has since become a dominant form of rice cultivation in China and has extended worldwide (Li et al., 2016). Despite initial challenges, such as seed purity issues and sensitivity to environmental conditions, subsequent improvements in hybrid rice breeding have led to the development of high-yielding varieties like ‘Liangyoupeijiu’ and ‘Liangyou E32’, which have been successfully commercialized and cultivated over large areas.

2.2 Basics and concept of heterosis

Heterosis, or hybrid vigor, refers to the phenomenon where hybrid offspring exhibit superior qualities compared to their parents. This concept has been extensively utilized in rice breeding to enhance yield and quality traits. Heterosis in rice is primarily achieved through the exploitation of genetic diversity between different subspecies, such as indica and japonica (Wu, 2009). The genetic basis of heterosis involves the interaction of multiple quantitative trait loci (QTLs) that cumulatively drive yield heterosis by regulating key yield components like spikelet number per panicle and effective panicle number (Li et al., 2016). Studies have identified specific heterosis-associated genes, such as qSS7 and qHD8, which contribute to the dominance effects observed in high-yielding hybrid varieties (Lin et al., 2020). The application of molecular biotechnology, including genome sequencing and marker-assisted selection, has further enhanced the understanding and utilization of heterosis in rice breeding.

2.3 Genetic basis of intersubspecific hybridization

Intersubspecific hybridization, particularly between indica and japonica rice varieties, has been a key strategy in developing high-yielding hybrid rice. This approach leverages the genetic diversity between the two subspecies to create hybrids with superior traits. The development of indica-japonica hybrids, such as ‘Yayou 2’, demonstrated the potential of intersubspecific heterosis to achieve high yields, although initial attempts faced challenges related to seed purity and environmental sensitivity (Li et al., 2005). Recent advancements have focused on developing parental lines with favorable genes from both subspecies, utilizing wide compatibility and thermosensitive genic male sterility (TGMS) genes to facilitate hybridization. The integration of molecular marker-assisted selection has enabled the identification and pyramiding of heterosis genes from different rice ecotypes, further enhancing the yield potential of hybrid rice. The success of China’s ‘super’ hybrid rice breeding project, which combines the ideotype approach with intersubspecific heterosis, underscores the effectiveness of this strategy in breaking the yield ceiling of irrigated rice crops (Peng et al., 2008).

3 Biological Basis of Intersubspecific Heterosis

3.1 Definition and types of intersubspecific heterosis

Intersubspecific heterosis, also known as hybrid vigor, refers to the phenomenon where hybrid progeny resulting from the cross between two different subspecies exhibit superior traits compared to their parents. This can manifest in various forms such as increased yield, enhanced growth rates, and improved resistance to diseases. The types of heterosis can be broadly categorized into three main genetic mechanisms: dominance, overdominance, and epistasis. Dominance refers to the masking of deleterious recessive alleles by dominant alleles, overdominance involves the superior performance of heterozygous genotypes over both homozygous parents, and epistasis is the interaction between different gene loci that results in enhanced performance (Zhang et al., 2008; Goff and Zhang, 2013; Fujimoto et al., 2018; Paril et al., 2023).

3.2 Genetic diversity and heterosis

Genetic diversity plays a crucial role in the manifestation of heterosis. The greater the genetic distance between the parental lines, the higher the potential for heterosis. This is because diverse genetic backgrounds can bring together a wide array of beneficial alleles and gene interactions. Studies have shown that the genetic basis of heterosis in rice involves multiple quantitative trait loci (QTLs) that cumulatively contribute to yield heterosis. For instance, the RH8 gene has been identified as a major QTL for yield heterosis in rice, highlighting the importance of specific genetic loci in driving hybrid vigor (Figure 1) (Huang et al., 2016; Li et al., 2016; Liu et al., 2020). Additionally, the presence of polymorphic promoter cis-regulatory elements and differential gene expression in hybrids further underscores the complex genetic interplay underlying heterosis.

Figure 1 Comparisons of F1 lines derived from PA64s/L54, PA64s/L53, PA64s/L55, PA64s/L90, and LYP9 lines. L54, L53, L55, and L90 were four CSSLs (Adopted from Liu et al., 2020) Image caption: a The physical map of the 9311 variety and the CSSLs harboring qHD8PA64s. b Comparison of 1000-grain weight of the four F1 lines and LYP9. c-g The seed length, width, length, width ratio, and level of chalkiness in LYP9 and PA64s/L90. h Image of the seeds of LYP9 and PA64s/L90 (Adopted from Liu et al., 2020)

3.3 Common intersubspecific hybrid combinations and their advantages and disadvantages

Several intersubspecific hybrid combinations have been developed to exploit heterosis in rice. One notable example is the hybrid combination Liang-you-pei 9 (LYP9), which has shown significant yield advantages due to better parent heterosis (BPH) of spikelet number per panicle (SPP) and paternal parent heterosis (PPH) of effective panicle number (EPN). Another example is the use of multiplex CRISPR-Cas9 genome editing to produce clonal diploid gametes and tetraploid seeds, enabling clonal propagation of F1 hybrids and maintaining their heterozygosity (Wang et al., 2019).

However, these hybrid combinations also come with certain disadvantages. The cost of hybrid seed production can be high, and the beneficial traits of hybrids may be lost in subsequent generations due to genetic segregation (Wang et al., 2019; Paril et al., 2023). Additionally, the complexity of genetic interactions and the need for precise genetic engineering pose significant challenges in the development and maintenance of high-yielding hybrid varieties (Fujimoto et al., 2018).

4 Genetic Basis and Breeding Strategies for High-Yield Traits

4.1 Key indicators and genetic basis of high-yield traits

High-yield traits in hybrid rice are primarily influenced by both additive and non-additive gene actions. Studies have shown that the additive variance is a significant component of the total genotypic variance, which is crucial for the selection of superior parental lines and hybrids (Gaballah et al., 2022). The principal component analysis (PCA) has identified key yield component traits, such as grain yield, spikelet number per panicle, and plant height, which are essential indicators of high yield (Duan et al., 2013). The genetic basis of these traits often involves complex interactions between multiple quantitative trait loci (QTLs) and specific alleles that contribute to heterosis, or hybrid vigor, resulting in superior performance of hybrids compared to their parents (Huang et al., 2015; Li et al., 2016; Liu et al., 2020).

4.2 Important yield-related genes and their functions

Several key genes have been identified as crucial for enhancing yield traits in hybrid rice. The Gn1a gene, which influences spikelet number per panicle, is a major determinant of grain yield. The DEP1 gene is associated with dense and erect panicle architecture, contributing to increased grain number and yield (Duan et al., 2013). Another important gene, Ghd7, plays a significant role in regulating heading date and plant height, which are critical for optimizing the growth period and maximizing yield potential (Li et al., 2016). These genes, along with others like Sd1 for plant height and IPA1 for ideal plant architecture, collectively contribute to the high-yield traits observed in hybrid rice varieties.

4.3 Application of molecular marker-assisted selection and gene editing in high-yield breeding

The integration of molecular marker-assisted selection (MAS) and gene editing technologies has revolutionized high-yield breeding in hybrid rice. MAS allows for the precise selection of desirable traits by identifying specific genetic markers linked to high-yield QTLs, thereby accelerating the breeding process (Qian et al., 2016). Gene editing tools, such as CRISPR/Cas9, enable targeted modifications of key yield-related genes, facilitating the development of rice varieties with enhanced yield potential. These advanced breeding strategies have unlocked the potential for rational design in rice breeding, combining wide-cross compatibility and intersubspecific heterosis to create superior hybrid varieties. The cumulative effects of these genetic components, including overdominance and epistatic interactions, are essential for achieving significant yield improvements in hybrid rice (Figure 2) (Luo et al., 2001; Zhou et al., 2022). Genetic engineering approaches, including CRISPR technologies, provide novel solutions to tackle fertility challenges in autotetraploid rice by targeting genes involved in meiosis and pollen development. Through CRISPR/Cas9-mediated knockout of genes like TMS9-1 and TMS5, researchers have observed significant effects on fertility and pollen formation (Zhu et al., 2024).

Figure 2  Gene module analysis (Adopted from Zhou et al., 2022) Image caption: (A) module hierarchical clustering diagram. Dynamic Tree Cut was used to divide modules according to clustering results. Merged Dynamics was used for module division after merging the modules with similar expression patterns according to the module similarity, and the subsequent analysis was carried out according to the merged modules; (B) histogram of the number of genes in each module. The horizontal axis represents each module, and the vertical axis represents the number of genes; (C) modular gene correlation heatmap. Each row and column represents a gene, and the darker the color of each point (white→yellow→red) represents stronger connectivity between the two genes corresponding to the row and column, that is, the stronger the Pearson correlation. (D) correlation graph of trait association. The abscissa is the trait, and the ordinate is the module. Red represents a positive correlation, and green represents a negative correlation; the darker the color is, the stronger the correlation. The number in the brackets represents a significant p-value, where the smaller the value is, the stronger the significance (Adopted from Zhou et al., 2022)

5 Recent Advances in Hybrid Rice

5.1 Latest varieties and their characteristics

Recent advancements in hybrid rice breeding have led to the development of several high-yielding varieties with improved traits. For instance, China has successfully developed new rice hybrids with super high-yielding potential by utilizing indica-inclined and japonica-inclined parental lines. These hybrids have been grown on a large scale, demonstrating significant improvements in yield and grain quality (Cheng et al., 2007). Another notable example is the development of intersubspecific hybrids such as ‘Liangyoupeijiu’ and ‘Liangyou E32’, which have exhibited grain yields higher than 10.5 t/ha and have been widely adopted due to their superior performance and adaptability. Additionally, the ideotype approach has been employed to create second-generation New Plant Type (NPT) lines that outperform first-generation lines and indica check varieties, further enhancing yield potential (Peng et al., 2008).

5.2 Breeding advances based on genomic selection (GS)

Genomic selection (GS) has revolutionized hybrid rice breeding by enabling the identification and selection of superior alleles associated with high yield and other desirable traits. A comprehensive genomic analysis of 1 495 elite hybrid rice varieties and their parental lines revealed numerous superior alleles that contribute to heterosis. This study identified 130 loci associated with 38 agronomic traits, highlighting the importance of accumulating rare superior alleles with positive dominance effects to achieve high yields (Huang et al., 2015). Moreover, marker-assisted selection has been effectively used to develop restorer lines carrying disease resistance genes, thereby increasing breeding efficiency and enhancing the genetic diversity of hybrid rice (Cheng et al., 2007).

5.3 Utilizing modern genomic tools to optimize intersubspecific heterosis and high-yield traits

Modern genomic tools have been instrumental in optimizing intersubspecific heterosis and high-yield traits in hybrid rice. The exploitation of wide compatibility (WC) systems, such as the S5 locus on chromosome 6, has facilitated successful hybridization between indica and japonica subspecies. Marker-assisted screening has identified several novel WC sources, which have been used to develop high-yielding intersubspecific hybrids with stable performance across different locations (Figure 3) (Kallugudi et al., 2022). Additionally, molecular biotechnology has enabled the identification and introduction of yield-enhancing genes from wild rice and the construction of autoregulated senescence-delaying genes, significantly improving the heterosis of hybrid rice (Wu, 2009). The rational design approach, which combines wide-cross compatibility and intersubspecific heterosis with rapid genome sequencing, has further unlocked the potential for creating high-yielding hybrid rice varieties (Azad et al., 2022).

6 Case Studies

6.1 Successful breeding of specific hybrid varieties and their performance

The breeding of hybrid rice varieties has seen significant advancements through the integration of intersubspecific heterosis and high-yield traits. For instance, the development of hybrid varieties such as Guang8A×Giza181 and II-32A×Giza179 has been achieved by crossing cytoplasmic male sterile (CMS) lines with restorer (R) lines. This strategy leverages both additive and non-additive gene actions, with additive variance being the main component of the total genotypic variance (Gaballah et al., 2022). Additionally, the use of wide compatibility (WC) systems, such as the S5n allele, has facilitated successful hybridization between indica and japonica subspecies, leading to the development of high-yielding hybrids like IRG137 and IRG143 (Kallugudi et al., 2022).

The agronomic traits contributing to the high yield of these hybrids include large panicle size, reduced tillering capacity, and improved lodging resistance. These traits have been emphasized in the breeding programs to meet the demand for heavy panicles and a large source supply (Peng et al., 2008). The integration of superior alleles through genomic analysis has also played a crucial role, with high-yielding hybrid varieties accumulating numerous rare superior alleles with positive dominance (Figure 4) (Huang et al., 2015). The specific combining ability (SCA) and general combining ability (GCA) analyses have identified the best combiners among the genotypes, further enhancing grain yield (Azad et al., 2022).

Figure 3 Combined biplots for multilocation performance wide compatible hybrids based on GGE biplot analysis on the most significant NPT related traits (Adopted from Kallugudi et al., 2022)

6.2 Breeding project based on whole genome selection

A breeding project based on whole genome selection involves the generation, sequencing, and phenotyping of a large number of hybrid lines. For example, a study involving 10 074 F₂ lines from 17 hybrid rice crosses aimed to understand the genetic basis of heterosis for yield traits (Huang et al., 2016). This project classified modern hybrid rice varieties into three groups, each representing different hybrid breeding systems.

The technical route for integrating interspecific hybrid vigor and high-yield traits includes the use of marker-assisted selection and the identification of quantitative trait loci (QTLs) for yield traits. In China, the development of super hybrid rice has been achieved by combining the ideotype approach with intersubspecific heterosis, resulting in hybrid varieties that produce significantly higher yields than traditional varieties. The use of wide compatibility genes and thermosensitive genic male sterility (TGMS) genes has further facilitated the breeding of high-yielding hybrids (Azad et al., 2022).

The achievements of this breeding project include the identification of key genomic loci that contribute to yield advantages and the development of high-yielding hybrid varieties with superior agronomic traits. The prospects for promotion and application are promising, with the potential for these hybrids to be grown on a large scale, thereby contributing to global food security (Huang et al., 2016).

6.3 Case analysis summary and inspiration

The case studies highlight the importance of integrating genetic and genomic tools in hybrid rice breeding. The success of breeding programs that combine intersubspecific heterosis with high-yield traits provides a blueprint for future efforts. The use of wide compatibility systems and marker-assisted selection can significantly enhance breeding efficiency and yield potential (Peng et al., 2008).

One of the main challenges in hybrid rice breeding is the cross incompatibility between indica and japonica subspecies. The identification and utilization of wide compatibility genes, such as the S5n allele, offer a solution to this problem (Kallugudi et al., 2022). Additionally, the complexity of heterosis and the need for a comprehensive understanding of the genetic basis of yield traits require ongoing research and innovation. The use of whole genome selection and advanced genomic tools can address these challenges and pave the way for the development of superior hybrid rice varieties (Huang et al., 2015).

7 Challenges and Opportunities in Integrating Intersubspecific Heterosis and High-Yield Traits

7.1 Biological and technical challenges

Integrating intersubspecific heterosis and high-yield traits in hybrid rice varieties presents several biological and technical challenges. One significant issue is the cross incompatibility between indica and japonica rice varieties, which hampers the exploitation of heterosis through intersubspecific hybridization. The wide compatibility (WC) system, particularly the S5 locus, plays a crucial role in overcoming this barrier, but the S5n allele that facilitates intercrossing is not widely distributed in the rice gene pool, necessitating the identification of diverse WC sources (Kallugudi et al., 2022). Additionally, the balance between achieving a higher degree of heterosis and managing increased reproductive isolation is delicate. The reduced seed setting rate in F₁ hybrids due to reproductive isolation negatively impacts grain production, making it essential to find an optimal genetic divergence index (GDI) for parental lines to maximize yield (Dan et al., 2014).

Figure 4 Genetic structure and heterozygosity of rice hybrid varieties. Image caption: (a) Plots of the first two principal components of 1,439 rice hybrid varieties. (b) NJ tree of 1 439 indica hybrids constructed from simple matching distances of whole-genome SNPs. (c) Distribution of whole-genome heterozygosity of all the hybrids. (d) Heterozygosity plots of whole-genome SNPs in indica hybrids. The Ho and the He ( by the Hardy-Weinberg equation) were calculated for each SNP in the rice genome. The thresholds for highly heterozygous SNPs (Ho-He>0.4) and extremely low-heterozygous SNPs (Ho-He<−0.4) are indicated by horizontal lines. S5 (Hybrid sterility-5) locus is indicated (Adopted from Huang et al., 2015)

7.2 Impacts of climate change and pests and diseases

Climate change poses a significant threat to rice production by altering growing conditions and exacerbating the prevalence of pests and diseases. The development of hybrid rice varieties that can withstand these challenges is critical. For instance, the introduction of genes from wild rice and the construction of autoregulated senescence delaying genes have shown promise in enhancing the resilience of hybrid rice to environmental stresses (Wu, 2009). However, the continuous evolution of pests and diseases requires ongoing research and adaptation of breeding strategies to ensure the sustainability of high-yield hybrid rice varieties.

7.3 Future research directions and the potential application of emerging technologies

Future research in hybrid rice breeding should focus on leveraging emerging technologies such as CRISPR/Cas9 and epigenetics to overcome existing challenges and enhance yield potential. CRISPR/Cas9 offers precise genome editing capabilities, allowing for the targeted introduction of beneficial traits and the elimination of undesirable ones. This technology can be used to enhance wide compatibility, improve resistance to pests and diseases, and increase tolerance to abiotic stresses. Epigenetic modifications, which involve changes in gene expression without altering the DNA sequence, also hold potential for improving hybrid rice performance by regulating key yield-related traits (Li et al., 2016).

Moreover, integrative approaches that combine phenomic, genomic, and transcriptomic analyses can uncover multiple heterosis-related loci and provide a comprehensive understanding of the molecular mechanisms driving yield heterosis. For example, the identification of quantitative trait loci (QTLs) and differentially expressed genes associated with yield components can inform the strategic design of hybrid rice breeding programs (Gaballah et al., 2022). By integrating these advanced technologies and methodologies, researchers can develop hybrid rice varieties that not only achieve high yields but also exhibit resilience to the challenges posed by climate change and biotic stresses.

8 Future Prospects and Conclusion

The future of hybrid rice research and breeding is poised to leverage advanced genomic tools and biotechnological innovations. The integration of high-resolution mapping and functional identification of heterosis-associated loci will continue to play a pivotal role in understanding the genetic basis of hybrid vigor. Additionally, the application of rational design in creating defined ideotypes, combined with rapid genome sequencing, is expected to unlock new potentials in rice breeding. The development of wide compatibility varieties (WCVs) and the utilization of diverse genetic resources will further enhance the breeding of superior intersubspecific hybrids. Moreover, the continuous improvement of plant types, such as heavy panicle type and super high yielding ideotype, will remain a focus to achieve super high yields.

Integrating intersubspecific heterosis with high-yield traits presents a promising avenue for achieving significant yield improvements in hybrid rice. The exploitation of intersubspecific heterosis through the development of indica-japonica intermediate parental lines and the introgression of favorable genes from both subspecies has shown considerable potential. The use of molecular marker-assisted selection to pyramid different heterosis genes from various rice ecotypes can further enhance hybrid vigor. Additionally, the identification and utilization of yield-enhancing genes from wild rice and the construction of autoregulated senescence delaying genes are expected to dramatically improve the heterosis of hybrid rice. The success of China's ‘super’ hybrid rice breeding, which combines the ideotype approach with intersubspecific heterosis, underscores the effectiveness of this strategy in breaking the yield ceiling.

The research on hybrid rice has yielded several key findings that underscore the potential of hybrid vigor in enhancing rice productivity. The genetic dissection of yield traits in elite hybrids has identified overdominance as a principal genetic basis of heterosis, suggesting complex genetic and biochemical mechanisms underlying hybrid vigor. The development of high-yielding hybrid varieties through the ideotype approach and intersubspecific heterosis has demonstrated significant yield advantages over traditional varieties. Furthermore, the identification of wide compatibility genes and the development of diverse WCVs have facilitated the breeding of superior intersubspecific hybrids. The integration of biotechnological interventions, such as molecular marker-assisted selection and the cloning of key enzymes related to the C4 pathway, has further enhanced the genetic enhancement and sustainability of hybrid rice.

Acknowledgments

We also thank the anonymous reviewers for their insightful comments and suggestions that greatly improved the manuscript.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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