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Article

Identification of QTLs Conferring Rice Leaf Inclination Angle and Analysis of Candidate Genes

by
Yiting Luo
1,†,
Qianqian Zhong
1,†,
Dian Yu
1,
Xuan Li
1,
Wenjing Yin
1,
Jinjin Lian
1,
Huimin Yang
1,
Mei Lu
1,
Sanfeng Li
2,
Weilin Zhang
1,*,
Yuexing Wang
2 and
Yuchun Rao
1
1
College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China
2
National Key Laboratory of Rice Biological Breeding, China National Rice Research Institute, Hangzhou 310006, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(12), 2891; https://doi.org/10.3390/agronomy13122891
Submission received: 7 November 2023 / Revised: 22 November 2023 / Accepted: 23 November 2023 / Published: 24 November 2023
Browse Figures
Versions Notes

Abstract

:
The leaf inclination angle is an important agronomic rice trait and an indicator of ideal plant architecture, yield and revenue. Based on 120 recombinant inbred lines (RILs) obtained from crossing of the F1 generation of the indica rice cultivar Huazhan as the male parent and the japonica rice cultivar Nekken2 as the female parent, followed by inbreeding for 12 generations, the leaf inclination angle of the first, second and third leaves from the top of the plants were analyzed. At the same time, quantitative trait locus (QTL) mapping of the leaf inclination angle was performed using encrypted genetic maps constructed for this population. A total of 33 QTLs were detected, including two related to the first leaf inclination angle (FLIA), nine related to the second leaf inclination angle (SLIA) (highest Lod value of 5.94), and 22 related to the third leaf inclination angle (TLIA) (highest Lod value of 8.53). At the same time, candidate genes analysis were conducted on the detected QTLs’ intervals, and a total of 15 candidate genes were screened. The expression levels of candidate genes were detected by RT-qPCR, we found that LOC_Os03g46920, LOC_Os03g52630, LOC_Os04g24328, LOC_Os08g25380, LOC_Os09g23200, LOC_Os09g32080, LOC_Os09g35940, LOC_Os09g37330 and LOC_Os09g37495 displayed extremely significant differences in expression between the parents. The results showed that these genes may be the cause of the difference in leaf inclination. The present study provided substantial foundation for the further validation of the function of leaf inclination angle genes and molecular breeding practices.

1. Introduction

Rice is one of the main crops in the world, and its yield plays a crucial role in global food security. With the increase in world population and the decrease in the tillable land area, the rice yield must be improved. Donald first proposed an ideal plant architecture to maximize plant photosynthetic efficiency that has since attracted research interest to improve rice architecture [1]. Japanese cultivator Matsushima Toshihiro, and Chinese rice breeders Shouren Yang and Longping Yuan, mentioned that erect rice leaves are the key plant type requirements for cultivating high-yield rice [2,3,4]. Afterwards, many scholars in China and other countries conducted extensive research on ideal plant types in order to achieve new breakthroughs in rice yield.
The leaf inclination angle, i.e., the angle between the leaf and stem, is an important agronomic trait, and an important component of the ideal plant type for rice. Numerous studies have shown that the plant architecture with erect leaves can effectively increase the light receiving area of the leaves, improve photosynthetic efficiency, and thus increase rice yield [5]. The agronomic traits of leaf inclination angle are closely related to the upright plant type of rice. Xuchu Sun [6] believed that the blade angle determined the light-receiving ability of the blade and that the light-interception effect on the lower layer influences photosynthesis. Chen et al. [7] believe that the growth angle of the top three leaves will affect the light reception of rice individuals and populations, thereby affecting the total photosynthetic production. A reasonable spatial distribution of the top three leaves can optimize the light reception posture, improve photosynthetic efficiency, and increase yield. Mantilla-Perez et al. [8] found that the size of plant leaf inclination angle plays a key role in light interception efficiency, photosynthetic rate, and yield, and it is the most important canopy structure parameter. Meanwhile, research has shown that smaller leaf inclination angle could also improve the effects of nitrogen accumulation in rice leaves on grain filling, which is of significance to rice yield and revenue [9,10]. Therefore, researching the regulatory mechanism of rice leaf inclination angle is of great significance for improving the photosynthetic rate and yield of rice.
Numerous molecular mechanisms to describe the leaf inclination angle have been proposed. It is universally acknowledged that hormones and nutritional status influence the inclination angle of rice leaves [11]. An increasing number of studies have shown that endogenous hormones play a major regulatory role in the formation of the rice leaf inclination angle, particularly brassinolide (BR), auxin (IAA), cytokinin (CTK), jasmonic acid (JA) and gibberellin (GA). The synthesis of these hormones and their abnormal signal transduction leads to an imbalance of cell growth and division on the proximal axial and distal axial surfaces of the pulvinus, further influencing the size of the leaf inclination angle [12]. BR exerted the most direct effects and other hormones regulate leaf inclination mainly by influencing BR [13]. The regulation of the leaf inclination angle is a complex process involving multiple genes and signaling pathways. Numerous rice leaf inclination-related genes associated with BR synthesis and signal transduction have been identified. Shimada et al. [14] suggested that OsSPY regulates GA and BR signaling. Bai et al. [15] inhibited OsBZR1 expression through RNAi silencing, which lead to changes in including rice dwarfing, upright leaves, reduced BR sensitivity and the expression of BR responsive genes, providing evidence of the role of OsBZR1 in the rice BR response. Song et al. [16] argued that OsIAA1 regulates the crosstalk between BR and IAA signal transduction. Zhao et al. [17] identified and cloned the LC2 gene, which is expressed in leaf joints during leaf development and plays an important role in hormone regulation and leaf inclination. Zhang et al. [18] found that rice cultivars with high OsARF19 expression have increased cell division at the proximal axial surface, resulting in increased leaf inclination. Huang et al. [19] found that OsCKX3 is highly expressed in the rice lamina joint, which mediates the accumulation of CTK, thereby controlling the development of rice lamina joint and negatively regulating leaf inclination angle.
Whilst an array of studies have described the molecular mechanisms of the leaf-inclination, they have focused on selected genes, and our current understanding of the genetic basis of rice leaf inclination angle remains incomplete. The rapid development of molecular marker technology provides a novel approach to identify the number of loci controlling quantitative traits. To date, an array of QTLs associated with the leaf inclination angle have been identified, the majority of which are associated with the flag leaf angle (FLA). Li et al. [20] identified FLA QTLs located on chromosomes 2, 5, 6, 7 and 9, respectively, and the QTLs on chromosomes 2 and 5 had relatively large effect sizes. Dong et al. [21] identified four QTLs controlling FLA on chromosomes 1, 2, 3 and 12, respectively, using indica rice Zhaiyeqing 8 and japonica rice Jingxi 17 and the DH population subsequently constructed. Kobayashi et al. [22] planted rice under different environmental conditions and detected six FLA-related QTLs. However, no QTLs were repeatedly detected across the different seasons and the corresponding effect sizes were small. It was concluded that the FLA is determined by environmental rather than genetic factors. Zhang et al. [23] detected five QTLs controlling FLA, located on chromosomes 1, 3, 5 and 11, in which two QTLs were detectable on chromosome 1. Luo et al. [24], using the japonica rice Taichung Native 1 and japonica rice Chunjiang 06 and their DH populations, detected five, four and four QTLs on the flag leaf, and on the second and third leaves from the top which were distributed on chromosomes 1, 3, 6, 8, 10 and 11. Hu et al. [25], using 863B and A7444 as materials, analyzed the genetic segregation of FLA and identified four QTLs controlling the angle of the flag leaf, located on chromosomes 2, 3 and 8, respectively, two of which were detected on chromosome 3. Cai et al. [26] investigated the DH population using the cross combination of indica rice ZYQ8 and japonica rice JX17 as materials, and detected nine QTLs controlling FLA, six of which were detected on chromosomes 1, 2, 2, 7, 9 and 12 in Hainan, and three were detected on chromosomes 6, 8 and 12 in Hangzhou. Jiang et al. [27] conducted a genome-wide association study on FLA in six different environments, and detected a total of six QTLs, of which one was a new locus that had not been studied by previous researchers, and verified the function of the candidate gene OsFLA2. Gui et al. [28] identified leaf angle during rice heading and detected a total of six QTLs in the past two years, of which five were reported for the first time. Rice researchers utilized different rice populations, genetic analysis and gene mapping of the rice leaf inclination angle has been performed in different environments, providing a solid foundation for aggregating rice leaf angle dominant alleles and improving rice plant types.
The majority of studies indicate that rice leaf angle is controlled by multiple genes, but the results from different studies have low comparability, and the contribution rate of some loci is low. In addition, the majority of studies examined only the FLA, and studies on the second and third leaves from the top of the plants are sparse. These three leaves (flag leaf, second and third leaves) are major components of rice photosynthesis during its later stages. In addition, the leaf angle is key to plant architecture breeding, which crucially impacts the rice yield. In this study, using the RILs population developed from the typical indica rice cultivar and japonica rice cultivar (Huazhan/Nekken2) we re-performed genetic analysis on the angle-controlling QTLs of the first leaf, and the second and third leaves from the top. In addition to QTL mapping we aimed to identify stable and reliable QTLs for molecular marker-assisted selection, which will lay a solid foundation for improving rice plant architecture and increasing plant yield.

2. Materials and Methods

2.1. Plant Materials

The F1 generation was obtained through the crossing of the indica rice cultivar Huazhan as the male parent and the japonica rice cultivar Nekken2 as the female parent. The F1 generation was self-crossed through artificial bag using the single seed descend method. After 12 generations of continuous self-crossing, 120 RILs with a relatively stable genotype and phenotype were obtained to form the genetic population (Figure 1).

2.2. Rice Planting and Management

A total of 60 seeds of each cultivar were selected, and seed surfaces were disinfected with 70% alcohol and 10% sodium hypochlorite for 10 min, followed by rinsing in deionized water, and soaking for 2 days in water, during which the water was changed one time. Seeds were then wrapped in a wet towel and placed in a 37 °C incubator to accelerate 48 h germination. The seeds with a consistent germination status were selected for sowing in the nursery field. One month later, 24 seedlings from each rice cultivar were selected for transplanting arranged as 4 rows and 6 columns. Regular field management was performed during this period, along with weeding and deinsectization.

2.3. Determination of the Leaf Inclination Angle

At the tillering-hearty-period of rice, a total of 5 tillers were randomly selected from each cultivar. The vertical tilting angle between the leaf vein and the stem of the first, and the second and third leaves from the top were measured using a goniometer. Data from each group were recorded and averaged.

2.4. Construction of Genetic Maps

The CTAB (Hexadecyltrimethylammonium bromide) method [29] was used to extract genomic DNA from young leaves of Huazhan, Nekken2, and 120 RILs. Barcode multiplex sequencing libraries were constructed as per the manufacturer’s recommendations (Illumina, San Diego, CA, USA), and paired-end sequencing was performed using the Illumina X-Ten sequencer (Illumina, San Diego, CA, USA) with 10× sequencing depth for 120 RILs and 50× for the RIL parents. Readings were aligned to the Nipponbare version 7 reference genome (http://rice.plantbiology.msu.edu/, accessed on 7 July 2023) using BWA MEM version 0.7.10 [30]. SNP calling and filtration were performed using SAMtools version 1.6 [31]. Circos version 0.67 was used to construct a circular ideogram that display complete genome variation information [32]. The variation sites among the RILs obtained from Huazhan and Nekken2 were compared, and their genotypes were determined using a hidden Markov model approach [33]. Consecutive SNP sites within the same genotype were clustered, with those less than 100 kb filtered out. Sequencing data was analyzed to obtain a total of 4858 markers evenly distributed in 12 chromosomes. Genetic maps were obtained [34].

2.5. QTL Localization and Analysis

Based on the high-density SNP molecular marker linkage map constructed in the laboratory, we performed QTL mapping on FLIA, SLIA and TLIA with Mapmaker/QTL1.1B (3.0) software using the interval mapping method. The LOD = 2.0 was set as the threshold to determine the existence of the QTL. QTLs were named based on the principles of McCouch et al. [35].

2.6. Quantitative Analysis of Gene Expression

Total RNA from leaves of the parental lines during the tillering stage was extracted using the TRIzol total RNA extraction kit (Invitrogen, Carlsbad, CA, USA), and RNA samples following DNase I treatment were reversely transcribed into cDNA using reverse transcription ReverTra Ace ®qPCR RT Kits (Toyobo, Shanghai, China). Based on the QTL localization data, the genes associated with leaf inclination were selected for phenotypic analysis in the interval between chromosomes 3, 4, 5, 6, 8 and 9. The expression of each individual gene in both parents was analyzed using reverse transcription-quantitative PCR (RT-qPCR). OsActin was used as the internal reference gene. All experiments were performed in triplicate and relative quantitative analysis was performed using the 2−ΔΔCT [36] method. Reactions were repeated 3 times. In the 7500 real-time PCR system (ABI, Shanghai, China), data were statistically analyzed using Excel 2016 and SPSS19.0 software. Data were compared for statistical differences using t-tests. The RT-qPCR reaction system was as follows: total volume 20 μL; cDNA 2 μL; SYBR qPCR Mix (Toyobo) 10 μL; forward and reverse primers (10 μmol·L–1) 0.8 μL each; and ddH2O to 20 μL. The RT-qPCR amplification procedure was as follows: 95 °C for 30 s, 95 °C for 5 s, 55 °C for 10 s, 72 °C for 15 s, with 40 cycles in total. Primer sequences are shown in Table 1. The gene expression levels of each treatment and control group were analyzed using Duncan’s multiple range test for the analysis of the statistical significance.

3. Results

3.1. Performance of the Leaf Inclination Angle in Parent and RILs

After measuring the leaf inclination angle of the first, second and the third leaves from the top of the plants of parents and RILs populations, we analyzed the data to determine that the parental leaves demonstrated different leaf inclination angles (Figure 2). The leaf inclination angle of the maternal plant Nekken2 was smaller, and the average values of the first, second and the third leaves from the top of the plants were 3.4°, 4.4° and 14.6°, respectively. The leaf inclination angle of the paternal plants were larger, with average values of 3.8°, 4.8° and 19.8°, respectively. The angle of the first, second and third leaves from the top of the RILs is shown in Figure 3. The obtained data conformed to a continuous normal distribution with a wide range. Many transgressive individuals showed genetic characteristics of quantitative traits, which was in line with the requirements for QTL interval mapping.

3.2. QTL Localization and Analysis

We performed QTL mapping using 4858-markers, which were evenly mapped to all 12 chromosomes. A total of 33 leaf inclination-related QTLs were detected (Table 2 and Figure 4), of which two were detected for FLIA and were located on chromosomes 4 and 9, respectively. For SLIA, a total of nine QTLs were detected, four of which were located on chromosome 3, three on chromosome 9, and chromosomes 6 and 8 each have one. A total of two QTLs on chromosome 9 had larger LOD values: 5.94 and 5.80, respectively. For TLIA, a total of 22 QTLs were detected, five of which were on chromosome 3, seven on chromosome 4, one on chromosome 5, six on chromosome 8, and three on chromosome 9. The QTL with the highest LOD value of 8.53 had a physical distance within the range of 17,448,080 to 22,938,953 on chromosome 9.

3.3. Expression Analysis of Rice Leaf Inclination-Related Genes

According to the interval distribution of QTLs related to the leaf inclination angle, we consulted the website of the Rice Genome Annotation Project (http://rice.plantbiology.msu.edu, accessed on 7 July 2023) and the Gene pool of the National Rice Data Center (http://www.ricedata.cn/gene/, accessed on 7 July 2023) and, combined with previous research results, 15 candidate genes possibly related to leaf inclination angle were preliminarily screened (Table 3). We compared the gene expression levels between parents by real-time fluorescent qPCR (Figure 5). The comparison showed that LOC_Os03g46920, LOC_Os03g52630, LOC_Os04g24328, LOC_Os08g25380, LOC_Os09g23200, LOC_Os09g32080, LOC_Os09g35940, LOC_Os09g37330 and LOC_Os09g37495 displayed extremely significant differences in expression between the parents. The expression levels of LOC_Os03g46920, LOC_Os03g52630, LOC_Os09g23200, LOC_Os09g32080 and LOC_Os09g37330 in Huazhan were extremely significant, higher than those of Nekken2, whilst the expression of LOC_Os04g24328, LOC_Os08g25380, LOC_Os09g35940 and LOC_Os09g37495 in Huazhan were extremely significant, lower than Nekken2. In addition, the genes LOC_Os04g21950 and LOC_Os08g06380 displayed significant differences in expression between the parents. The expression levels of LOC_Os08g06380 in Huazhan were significantly higher than those of Nekken2, whilst the expression of LOC_Os04g21950 in Huazhan was significantly lower than Nekken2. Significant differences in the expression levels of these genes between both parents indicates their involvement in leaf inclination angle.

4. Discussion

The leaf inclination angle of rice is a quantitative trait controlled by multiple genes. Different rice populations, growth environments and treatment methods influence the results of QTL mapping. Previous studies assessed leaf-inclination-related QTLs of rice using different rice populations, the majority of which were related with FLA. Cai et al. [26] used the ZYQ8/JX17-DH population, and localized a QTL controlling the FLA within the marker interval from CT195 to G1073 of chromosome 8. Hu et al. [25] identified a QTL controlling the FLA within the marker interval from RM6215 to RM8265. These two QTLs partially overlapped with the qTLIA8-4 interval obtained in this study, so there may be a pleiotropic locus in this interval, simultaneously affecting both FLA and TLIA. Luo et al. [24], using the TN1/CJ06-DH population, discovered a pleiotropic locus that simultaneously controls the FLIA, SLIA and TLIA within the marker interval from RM4085 to RM1111 chromosome 8, which coincided with the qTLIA8-5 detected in this study. This indicated that at least one gene regulated the rice leaf inclination angle within this interval. Dong et al. [46] used the GWAS to detect QTL intervals related to FLA, the qFLA8f (20968463–21468267 bp) located on chromosome 8 was adjacent to qTLIA8-6, which controlled TLIA as detected in this study, the qFLA3e (21294778–22460027 bp) detected on chromosome 3 was similar to the qTLIA3-1 that controls TLIA detected in this study. Therefore, it is speculated that there may be effector sites controlling leaf inclination angle near these two intervals. Jiang et al. [27] studied the phenotypic values of FLA in 353 rice germplasm under six different environments and obtained six QTLs. Among them, qFLA4 located on chromosome 4 partially overlaps with qTLIA4-2 in this study, suggesting that there may be a controlling leaf inclination near this site. Dong et al. [47] conducted GWAS on rice FLA data for two consecutive years, using this data with 262 simple sequence repeat (SSR) markers, and identified seven FLA related marker loci. The marker site RM6997 is located within the qTLIA4-5 locus obtained in this study, and RM6215 is located within the qTLIA8-5 locus detected in this study. The RM4835 marker site on chromosome 4 is similar in distance to qTLIA4-1, and RM4835 has been continuously detected for two years. There are high possibility of genes controlling rice leaf inclination angle near these loci, which have significant research value. We thus validated the results of previous studies and further demonstrated the value of these QTLs obtained.
We obtained multiple new loci in this study. qTLIA9-3 with an LOD value of up to 8.53 was localized within the interval at a physical distance of 17448080–22938953 on chromosome 9; this indicated that there was likely to be a major gene controlling the inclination of the third leaf from the top of the plant within this interval, which could improve the rice cultivars. Two other loci with larger LOD values also localized on chromosome 9; qSLIA9-1 and qSLIA9-3. qSLIA9-1 had LOD values of 5.94, and were localized within the interval at a physical distance of 7423269–9911482 on chromosome 9; qSLIA9-3 had a LOD value of 5.80 and was localized within the interval at a physical distance of 18564963–22938953. As shown in Figure 3, the QTLs discovered on chromosome 9 not only had larger LOD values, but also overlapped with the interval of the QTL of the inclination angle of the first, second and third leaves from the top. For example, qSLIA9-1 and qTLIA9-1 are located in the same region, qSLIA9-2 and qTLIA9-2 are overlapped, and qFLIA9-1, qSLIA9-3 and qSLIA9-3 were also located within the same area, indicating the presence of a pleiotropic gene controlling the inclination angle of all leaves assessed.
Previous studies have shown that the leaf inclination angle trait in rice is regulated by multiple genes. According to the QTLs detected in this study and the rice genome database (http://rice.plantbiology.msu.edu/, accessed on 7 July 2023), we have screened a total of 15 candidate genes that may be related to the leaf inclination angle trait. The genes related to the rice leaf inclination angle are mainly related to hormones, especially BR, as well as hormones such as GA, JA, IAA, etc. [48]. LOC_Os03g49620 encodes BR INSENSITIVE 1-associated receptor kinase 1 precursor; LOC_Os08g25380 is a homeotic gene of BR receptor kinase coding gene OsBRI1 [40]. BR plays multiple roles in the growth and development of rice, and applying BR alone can promote the bending of the junction between leaf and stem [49], controlling the size of the rice leaf inclination angle. LOC_Os04g24328 encodes JA-induced protein, JA can inhibit the synthesis of BR and its signaling pathway, thus indirectly regulating the size of the rice leaf inclination angle [50]. LOC_Os09g35940 is a cytochrome P450 gene, the cytochrome P450 family plays a key role in BR biosynthesis, and will affect plant type traits such as leaf inclination angle and seed size [51]. In previous studies, a number of genes related to leaf inclination angle encode cytochrome P450, such as OsCPD2, OsCPD1 and D11 [52,53]. LOC_Os09g37330 is small auxin-up RNA (SAUR) gene, and acts as a negative regulator of auxin synthesis and transport in rice [45]. LOC_Os09g37495 encodes auxin responsive protein. Auxin plays a crucial role in regulating the size of leaf inclination angle, as it can regulate the growth of the proximal axial and distal axial surfaces of the pulvinus [54]. Therefore, LOC_Os09g37330 and LOC_Os09g37495 may regulate leaf inclination angle by regulating auxin content. In addition to being regulated by hormones, the mechanical tissue strength of rice leaves is also one of the key factors affecting leaf inclination angle size [13]. LOC_Os03g52630 is a glycoside hydrolase gene; it is involved in the biosynthesis of cellulose in rice, and it affects the mechanical strength of rice [37]. LOC_Os08g06380 encodes cellulose synthase-like F; research has shown that this gene mediates the biosynthesis of cell wall polysaccharides, thereby affecting the mechanical properties of the cell wall, making the cell wall of rice stems more fragile [41]. LOC_Os08g01330 encodes NAC transcription factor; NAC transcription factors play a key role in the regulation of secondary wall biosynthesis, thereby affecting the mechanical strength of plants [55]. LOC_Os08g28860 and LOC_Os09g38040 encode Nudix hydrolase; it can specifically hydrolyze ADP ribose in the cytoplasm, leading to downregulation of genes related to lignin biosynthesis [56], thereby reducing the mechanical strength of the plant. LOC_Os09g32080 encodes a chitinase-like protein, which is necessary for cellulose biosynthesis and will affect plant mechanical strength [44]. These candidate genes can all affect the mechanical strength of rice plants, thus potentially affecting the leaf inclination angle of rice. LOC_Os09g29130 is a Zn-finger transcription factor, it will induce rice leaves to curl towards abaxially curled. And, to some extent, it will affect the size of leaf inclination angle [43]. Like LOC_Os09g29130, LOC_Os09g23200 is also a leaf curling gene that regulates rice leaf curvature by regulating the development of adaxial cells in the leaf, thus the gene also regulate the leaf inclination angle of rice [42]. LOC_Os04g21950 encodes a DNA binding protein that contains one WRKY domain, it is involved in the regulation of multiple life processes, it plays a key role in JA response and GA-mediated seed development, aging, abiotic stress and other development processes [57,58], playing a key role in regulating the angle of leaves.
This study identified 33 QTLs related to rice leaf inclination angle traits by studying the RILs population developed by Huazhan and Nekken2. Combining these QTLs and rice genome database (http://rice.plantbiology.msu.edu/, accessed on 7 July 2023), a total of 15 candidate genes that may be related to leaf inclination angle traits were identified. Leaf inclination angle affects the surface area of rice leaves exposed to light, thereby affecting rice yield. In rice breeding, regulating the leaf inclination angle is the key to creating an ideal plant type of rice. Thus, these results provide foundation for future molecular breeding practices. Once these genes have been confirmed, they can be used modify and improve plant architecture and yield.

Author Contributions

Conceptualization, Y.R., W.Z. and Y.W.; methodology, Y.L. and Q.Z.; software, Q.Z., D.Y. and W.Y.; data curation, H.Y., X.L., D.Y. and J.L.; writing—original draft preparation, Y.L., Q.Z. and J.L.; writing—review and editing, Q.Z., W.Y., M.L. and Y.R.; supervision, S.L., Y.R., W.Z. and Y.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Zhejiang Provincial Natural Science Foundation of China (Grant No. LZ23C130003), the National Key R&D Program of China (Grant No: 2021YFA1300703), and Hainan Yazhou Bay Seed Lab (Grant No. B21HJ0219).

Data Availability Statement

We obtained the QTL mapping and function information of candidate genes from rice gene database (http://rice.plantbiology.msu.edu/, accessed on 7 July 2023), (http://www.ricedata.cn/gene/, accessed on 7 July 2023). All other data supporting this result are included in the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 13 02891 g001
Figure 1. Construction of RILs population.
Figure 1. Construction of RILs population.
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Figure 2. The leaf inclination angle of the first, second and third leaves from the top in parents, the bar = 1 cm. (A) The leaf inclination angle of the first leaf from the top in parents; (B) the leaf inclination angle of the second leaf from the top in parents; (C) the leaf inclination angle of the third leaf from the top in parents.
Figure 2. The leaf inclination angle of the first, second and third leaves from the top in parents, the bar = 1 cm. (A) The leaf inclination angle of the first leaf from the top in parents; (B) the leaf inclination angle of the second leaf from the top in parents; (C) the leaf inclination angle of the third leaf from the top in parents.
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Figure 3. Distribution of the leaf inclination angle of the first, second and third leaves from the top in rice recombinant inbred lines (RILs) population. (A) The first leaf; (B) the second leaf; (C) the third leaf.
Figure 3. Distribution of the leaf inclination angle of the first, second and third leaves from the top in rice recombinant inbred lines (RILs) population. (A) The first leaf; (B) the second leaf; (C) the third leaf.
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Figure 4. Mapping of leaf inclination angle QTLs in RILs population.
Figure 4. Mapping of leaf inclination angle QTLs in RILs population.
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Figure 5. Expression of leaf inclination angle related genes in rice. * representsa significant difference at the p < 0.05 level; ** represents a significant difference at the p < 0.01 level.
Figure 5. Expression of leaf inclination angle related genes in rice. * representsa significant difference at the p < 0.05 level; ** represents a significant difference at the p < 0.01 level.
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Table 1. Primer sequences of real-time fluorescent quantitative PCR.
Table 1. Primer sequences of real-time fluorescent quantitative PCR.
Primer NameSequence (5′–3′)Tm (°C)Length (bp)Amplicon Length (bp)
LOC_Os03g49620-F-qrtGCAAGGAAACGTGTGGCAAT60.0020153
LOC_Os03g49620-R-qrtCTTTGCCAGGCCAAAGTCAC60.0020
LOC_Os03g52630-F-qrtCATGCTCAGCTGGAGTGTGA60.0020166
LOC_Os03g52630-R-qrtGTCACCTACACCCACCTGTG60.0020
LOC_Os04g24328-F-qrtTCAAGGACTGGTACGGCAAC60.0020172
LOC_Os04g24328-R-qrtGACTTGTGGACGTGGTGGAA60.2020
LOC_Os04g21950-F-qrtCCATGGATCTGATGGGTGGG59.9020181
LOC_Os04g21950-R-qrtGTGATCTCCCTGCAGTCCAC60.1020
LOC_Os08g01330-F-qrtTCAGCTACAAGGACCGCAAG60.0020158
LOC_Os08g01330-R-qrtGCGACCCTTGTAGAACACCA60.0020
LOC_Os08g25380-F-qrtTGGGGACTTCGTCGAAACTG60.0020191
LOC_Os08g25380-R-qrtACGGCAATGATGAGCACAGA60.0020
LOC_Os08g28860-F-qrtACATCTGAGGAGCGCGAAAA60.0020162
LOC_Os08g28860-R-qrtTCTTCGCTCGGGAAAGTCTG59.8020
LOC_Os08g06380-F-qrtCCGTCTTCCGTACCGAGAAG59.9020178
LOC_Os08g06380-R-qrtCACGAGAACCCGAACCAGAA60.0020
LOC_Os09g23200-F-qrtGAGCAACTCCTCAAGGGACC60.0020179
LOC_Os09g23200-R-qrtAGTCAGGCCTCCCTAGAGTG60.0020
LOC_Os09g29130-F-qrtCCCAGGAGCAGAAGGACAAG60.0020156
LOC_Os09g29130-R-qrtCCAGGGTGTGCTTGTTGTTG59.9020
LOC_Os09g32080-F-qrtCCATCCCCGTCTTCTGGAAC60.1020151
LOC_Os09g32080-R-qrtTGCTTCTTCTTCATCGGCGT60.0020
LOC_Os09g35940-F-qrtAATGGGTTCGGATCTCAGGC59.8020186
LOC_Os09g35940-R-qrtATCTCGCACGACAGCCTTAG59.9020
LOC_Os09g37330-F-qrtGAGAGCGATTTGGGGTTCCA60.0020200
LOC_Os09g37330-R-qrtGACAGAGCTCACAACAGCCT60.0020
LOC_Os09g37495-F-qrtGTCTTCGGCGAGCTTCTGAT60.2020167
LOC_Os09g37495-R-qrtCTCGCCATGGAGCTCAAGAA60.1020
LOC_Os09g38040-F-qrtGCCTTTGGACTCTTCCTGCT60.0020192
LOC_Os09g38040-R-qrtCAGGTGAGAAGTTGGGGGTC60.0020
Table 2. QTL interval statistics of leaf angle in rice in RILs population.
Table 2. QTL interval statistics of leaf angle in rice in RILs population.
TraitQTLChromosomePhysical Gap (bp)Position of Support (cM)LOD
First leaf inclination angleqFLIA4-10432047360–32418113137.38–138.972.10
qFLIA9-10920272099–2206612286.90–94.593.20
Second leaf inclination angleqSLIA3-10328166873–28398636120.74–121.742.02
qSLIA3-20328698205–28928756123.02–124.012.47
qSLIA3-30329344947–29512289125.79–126.512.11
qSLIA3-40330106459–30262983129.06–129.732.43
qSLIA6-10619814308–1995024384.94–85.522.72
qSLIA8-10837535–4847850.16–2.122.65
qSLIA9-1097423269–991148231.82–42.495.94
qSLIA9-20912363787–1254257953.00–53.772.02
qSLIA9-30918564963–2293895379.58–98.335.80
Third leaf inclination angleqTLIA3-10322963993–2366150598.44–101.432.33
qTLIA3-20325165251–25766328107.88–110.452.38
qTLIA3-30332267773–32435017138.32–139.042.71
qTLIA3-40332567335–32870078139.61–140.902.02
qTLIA3-50333386000–33510684143.12–143.652.57
qTLIA4-1043995063–414749317.13–17.782.18
qTLIA4-2044739169–488618120.32–20.952.20
qTLIA4-3046022948–645166625.82–27.662.15
qTLIA4-4047872497–1348309233.75–57.802.43
qTLIA4-50413890841–1503566059.55–64.452.33
qTLIA4-60415898826–1614682968.15–69.222.21
qTLIA4-70417276270–1758497574.06–75.382.38
qTLIA5-10528058252–28807595120.28–123.492.81
qTLIA8-108712661–10103533.05–4.332.37
qTLIA8-2081306603–16106655.60–6.902.50
qTLIA8-3083547205–369743115.21–15.852.33
qTLIA8-4087718778–891756433.09–38.232.35
qTLIA8-5089263931–1923563439.71–82.462.64
qTLIA8-60820195421–2043044486.57–87.582.32
qTLIA9-1097782000–998922633.36–42.823.21
qTLIA9-20912363787–1379117953.00–59.122.41
qTLIA9-30917448080–2293895374.80–98.338.53
Table 3. Rice leaf inclination angle candidate genes and their functions.
Table 3. Rice leaf inclination angle candidate genes and their functions.
Gene NumberChromosomeQTLFunctionsCloned or Not
LOC_Os03g496203qSLIA3-1BR INSENSITIVE 1-associated receptor kinase 1 precursorNot cloned
LOC_Os03g526303qSLIA3-4glycoside hydrolaseHave been cloned [37]
LOC_Os04g243284qTLIA4-5JA-induced proteinNot cloned
LOC_Os04g219504qTLIA4-4WRKY transcription factorHave been cloned [38]
LOC_Os08g013308qSLIA8-1NAC Transcription FactorHave been cloned [39]
LOC_Os08g253808qTLIA8-5BR receptor kinaseHave been cloned [40]
LOC_Os08g288608qTLIA8-5NUDIX hydrolaseNot cloned
LOC_Os08g063808qTLIA8-3cellulose synthase-like FHave been cloned [41]
LOC_Os09g232009qTLIA9-2SHAQKYF class MYB family transcription factorHave been cloned [42]
LOC_Os09g291309qTLIA9-3Zn-finger transcription factorHave been cloned [43]
LOC_Os09g320809qSLIA9-3qTLIA9-3membrane-associated chitinase-like proteinHave been cloned [44]
LOC_Os09g359409qFLIA9-1qSLIA9-3qTLIA9-3cytochrome P450Not cloned
LOC_Os09g373309qFLIA9-1qSLIA9-3qTLIA9-3small auxin-up RNA geneHave been cloned [45]
LOC_Os09g374959qFLIA9-1qSLIA9-3qTLIA9-3auxin responsive proteinNot cloned
LOC_Os09g380409qFLIA9-1qSLIA9-3qTLIA9-3NUDIX hydrolaseNot cloned
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Luo, Y.; Zhong, Q.; Yu, D.; Li, X.; Yin, W.; Lian, J.; Yang, H.; Lu, M.; Li, S.; Zhang, W.; et al. Identification of QTLs Conferring Rice Leaf Inclination Angle and Analysis of Candidate Genes. Agronomy 2023, 13, 2891. https://doi.org/10.3390/agronomy13122891

AMA Style

Luo Y, Zhong Q, Yu D, Li X, Yin W, Lian J, Yang H, Lu M, Li S, Zhang W, et al. Identification of QTLs Conferring Rice Leaf Inclination Angle and Analysis of Candidate Genes. Agronomy. 2023; 13(12):2891. https://doi.org/10.3390/agronomy13122891

Chicago/Turabian Style

Luo, Yiting, Qianqian Zhong, Dian Yu, Xuan Li, Wenjing Yin, Jinjin Lian, Huimin Yang, Mei Lu, Sanfeng Li, Weilin Zhang, and et al. 2023. "Identification of QTLs Conferring Rice Leaf Inclination Angle and Analysis of Candidate Genes" Agronomy 13, no. 12: 2891. https://doi.org/10.3390/agronomy13122891

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