Breeding for Heat Tolerant Aromatic Rice Varieties and Identification of Novel QTL Regions Associated with Heat Tolerance During Reproductive Phase by QTL-Seq

doi:10.1016/j.rsci.2024.12.002

Abstract

Abstract:

Extremely high temperatures resulting from climate change have become a major challenge for increasing rice production. Therefore, our objective was to develop heat-tolerant aromatic rice varieties using the pedigree method, focusing on selecting for seed-setting ability under extremely high temperatures along with the use of single nucleotide polymorphism/insertion and deletion (SNP/InDel) markers to improve aromatic properties and grain quality. Furthermore, the QTL-seq approach was utilized to identify QTLs for seed-setting rate in an F₂ population subjected to heat stress. The candidate QTL regions were then aligned to confirm SNPs/InDels in synonymous F₇ candidate heat-tolerant lines. The results revealed that four promising lines, namely 84-7-1-9, 84-7-1-10, 159-3-3-1, and 159-3-3-10, were classified as heat-tolerant with low amylose content. In addition, lines 84-7-1-9 and 84-7-1-10 were identified as aromatic rice encompassing the aroma gene (badh2). Regarding the QTL-seq results, the qSF2.1 region ranged from 311 051 to 3 929 422 bp on chromosome 2, was identified based on the highest contrasting SNP index between the heat-susceptible and tolerant bulks. The candidate genes within this region include two genes related to heat shock proteins, three genes associated with pollen fertility, and four genes involved in heat stress and other abiotic stress responses. These genes are proposed as potential candidates for heat tolerance and could serve as targets in rice breeding programs aimed at enhancing heat tolerance.

Key words: rice, heat stress, aroma, QTL-seq

Surangkana Chimthai, Sulaiman Cheabu, Wanchana Aesomnuk, Siriphat Ruengphayak, Siwaret Arikit, Apichart Vanavichit, Chanate Malumpong. Breeding for Heat Tolerant Aromatic Rice Varieties and Identification of Novel QTL Regions Associated with Heat Tolerance During Reproductive Phase by QTL-Seq[J]. Rice Science, 2025, 32(1): 67-80.

Figures/Tables 9

Fig. 1. Seed-setting rate, grain yield, and brown plant- hopper resistance of candidate lines in F6 and F7 generations. A, Seed-setting rates of 12 candidate lines in F6 and F7 generations. B, Grain yields of 12 candidate lines in F7 generation under field conditions. C, Scores of brown planthopper (BPH) resistance in F7 generation under controlled greenhouse. Kamphaeng Phet (KPP), Pak Hai (PH), Ta Phaya (TPY), and Sing Buri (SBR) are four brown planthopper biotypes. SES, Standard evaluation system. Sinlex, RH (Ratuhinati), and TN1 were used as heat susceptible, BPH resistance, and BPH susceptible checks, respectively. Different letters above the bars indicate significant differences at the 0.05 level using least significant difference.

Table 1. Single nucleotide polymorphism/insertion and deletion (SNP/InDel) marker information on 12 breeding lines identified in F7 generation and their parents.

Line/ Variety	Aroma (badh2)	Amylose content (wx^b)	Gelatinization temperature (SSIIa)	Brown planthopper
Line/ Variety	Aroma (badh2)	Amylose content (wx^b)	Gelatinization temperature (SSIIa)	TPS	Bph3
83-8-3-2	-/-	-/-	+/+	+/+	+/+
83-8-3-5	-/-	-/-	+/+	+/+	+/+
83-8-5-3	-/-	-/-	+/+	+/+	+/+
83-8-5-4	-/-	-/-	+/+	+/+	+/+
83-8-5-6	-/-	-/-	+/+	+/+	+/+
83-8-5-7	-/-	-/-	+/+	+/+	+/+
83-8-5-8	-/-	-/-	+/+	+/+	+/+
84-7-1-5	-/-	-/-	+/+	+/+	+/+
84-7-1-9	+/+	+/+	-/+	+/+	+/+
84-7-1-10	+/+	+/+	-/-	+/+	+/+
159-3-3-1	-/-	+/+	-/-	+/+	+/+
159-3-3-10	-/-	+/+	-/-	+/+	+/+
PTT1	+/+	+/+	+/+	+/+	+/+
M9962	-/-	-/-	-/-	+/+	+/+

Fig. 2. Principal component analysis (PCA) of 12 candidate lines and their parents to show genetic relationships obtained from whole-genome sequences.

Fig. 3. Plant type, alkaline test, milled grain, brown grain, and paddy grain of four promising lines in F7 generation compared with their parents (Pathumthani 1 and M9962).

Table 2. Grain size, alkalinity, chalkiness, amylose content, and 2-acetyl-1-pyrroline (2AP) content of four promising heat-tolerant lines (F7 generation) compared with those of their parents under controlled greenhouse and field conditions.

Line/ Variety	Milled grain width (mm)		Milled grain length (mm)		Chalky grain rate (%)		Alkaline score		Amylose content (%)		2AP content (mg/kg)
Line/ Variety	GH	Field	GH	Field	GH	Field	GH	Field	GH	Field	GH	Field
84-7-1-9	2.04 a	2.15 a	6.89 b	7.10 b	12.7 b	10.5 b	5 a	5 a	16.63 b	16.89 b	1.81 a	3.71 a
84-7-1-10	1.95 b	2.10 b	7.11 a	7.18 b	13.3 b	10.8 b	2 b	2 b	15.83 b	16.00 b	1.52 b	3.39 b
159-3-3-1	1.95 b	2.10 b	6.64 c	6.85 c	8.7 c	8.0 c	2 b	2 b	16.63 b	16.93 b	0.00 c	0.00 c
159-3-3-10	1.93 b	2.10 b	6.62 c	6.73 c	11.5 b	10.7 b	2 b	2 b	16.67 b	16.85 b	0.00 c	0.00 c
Pathumthani 1	1.92 b	2.00 c	7.30 a	7.38 a	8.2 c	7.0 c	5 a	5 a	16.00 b	16.50 b	1.78 a	3.55 b
M9962	2.01 a	2.08 a	6.54 c	6.50 d	29.6 a	20.2 a	1 b	1 b	25.73 a	25.80 a	0.00 c	0.00 c
F test (P < 0.05)	*	*	*	*	*	*	*	*	*	*	*	*
CV (%)	1.16	2.56	1.39	3.21	8.31	10.58	0.50	0.42	10.5	11.2	9.42	7.25

Fig. 4. QTL-seq analysis revealed a putative QTL region on chromosome 2. A, Sliding window plots of the single nucleotide polymorphism (SNP) index for two bulks (HT-bulk and HS-bulk) and a comparison of the ∆(SNP index) between them. (a) Pseuedomolecules of the Nipponbare reference genome (IRGSP 1.0). (b) Upper probability values at the 99% confidence level (P < 0.01). (c) Upper probability values at the 95% confidence level (P < 0.05). (d) Sliding window plots of ∆(SNP index). (e) Lower probability values at the 95% confidence level (P < 0.05). (f) Lower probability values at the 99% confidence level (P < 0.01). (g) Sliding window plots of the average SNP index values in the HT-bulk. (h) Sliding window plots of average SNP index values in the HS-bulk. (i) Candidate genomic regions containing QTLs for the seed-setting rate. B, SNP index and candidate genes on chromosome 2. Plots of the SNP index of SNPs in the HT-bulk (top; green dots) and HS-bulk (middle; orange dots), and plots of the Δ(SNP index) (blue dots) for the two bulks (HT-bulk and HS-bulk). Sliding window plots of the average SNP index, with a 500-kb window size and 10-kb steps, are presented as red lines. The pairs of orange and green lines in the Δ(SNP index) plots represent the 95% and 99% confidence intervals, respectively. The orange shading highlights the detected QTL region.

Table 3. QTL detected for the seed-setting rate in rice on chromosome 2.

QTL	Chromosome	Start (bp)	End (bp)	Interval (bp)	Δ(SNP-index)	HT-bulk SNP-index	HS-bulk SNP-index
qSF2.1	2	311 051	3 929 422	3 618 371	0.94	0.94	0.25

Fig. 5. Candidate genes on chromosome 2 and synonymous single nucleotide polymorphisms/insertions and deletions (SNPs/InDels) among F7 candidate lines, M9962, PTT1, HT-bulk, and HS-bulk. A, Candidate genes within the QTL regions. B, Genes containing synonymous SNPs/InDels among the candidate lines, heat-tolerant parent (M9962) and HT-bulk are highlighted in yellow. HT, Heat tolerant; HS, Heat sensitive; PTT1, Pathumthani 1; PSL2, Phitsanulok.

Table 4. Candidate genes that may be related to heat tolerance during the reproductive stage in qSF2.1 region.

Gene name	Functional domain and trait ontology	Pathumthani 1 allele	M9962 allele	HT-bulk allele	HS-bulk allele	F₇ allele
Os02g0115900	Endoplasmic reticulum-localized chaperone HSP70	ATG/ATG	A/A	A/A	ATG/ATG	A/A
Os02g0120800	GTPase, salt tolerance, negative regulation of disease resistance, pollen germination	AGG/AGG	A/A	A/A	AGG/A	A/A
Os02g0121000	Glutamyl-tRNA synthetase, responsible for thermosensitive chlorophyll-deficient phenotype in cde1(t) mutant	G/G	A/A	A/A	G/A	A/A
Os02g0121300	Cyclophilin-like domain, auxin signal transduction, heat tolerance	T/T	C/C	C/C	T/T	C/C
Os02g0122400	Similar to plastid division protein	A/A	G/G	G/G	G/A	G/G
Os02g0126400	Calcium-dependent protein kinase, positive regulator of salt and drought stress responses	A/A	C/C	C/C	A/A	C/C
Os02g0128400	Heat shock protein DnaJ domain protein B3 (HSP40), N-terminal domain-containing protein	TA/TA	T/T	T/T	T/TA	T/T
Os02g0141300	Arabinokinase-like protein, pollen development	C/C	T/T	T/T	C/C	T/T
Os02g0149800	Stress-responsive NAC1-regulated protein phosphatase, drought and oxidative stress tolerance	CTTTT/CTTTT	CTT/CTT	CTT/CTT	CTTTT/CTTTT	CTT/CTT

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