Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

Yumin Yang; Hongshen Wan; Fan Yang; Chun Xiao; Jun Li; Meijin Ye; Chunxiu Chen; Guangmin Deng; Qin Wang; Aili Li; Long Mao; Wuyun Yang; Yonghong Zhou

doi:10.1371/journal.pone.0234882

. 2020 Jun 25;15(6):e0234882. doi: 10.1371/journal.pone.0234882

Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

Yumin Yang ^1,^2,^3,^#, Hongshen Wan ^3,^4,^#, Fan Yang ¹, Chun Xiao ², Jun Li ^3,⁴, Meijin Ye ¹, Chunxiu Chen ², Guangmin Deng ², Qin Wang ^3,⁴, Aili Li ⁵, Long Mao ⁵, Wuyun Yang ^3,^4,^*, Yonghong Zhou ^1,^*

Editor: Aimin Zhang⁶

PMCID: PMC7316292 PMID: 32584908

Abstract

Strong early vigour plays a crucial role in wheat yield improvement by enhancing resource utilization efficiency. Synthetic hexaploid wheat (SHW) combines the elite genes of tetraploid wheat with Aegilops tauschii and has been widely used in wheat genetic improvement for its abundant genetic variation. The two SHWs Syn79 and Syn80 were derived from the crossing of the same tetraploid wheat DOY1 with two different Ae. tauschii accessions, AT333 and AT428, respectively. The Syn80 possessed better early vigour traits than Syn79, theretically caused by their D genome from Ae. tauschii. To dissect their genetic basis in a hexaploid background, 203 recombinant inbred lines (RILs) derived from the cross of Syn79 x Syn80 were developed to detect quantitative trait loci (QTL) for four early biomass related traits: plant height (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) per plant, under five different environmental conditions. Determined from the data of SNP markers, two genome regions on 1DS and 7D were stably associated with the four early biomass related traits showing pleiotropic effects. Four stable QTLs QPh.saas-1DS, QTn.saas-1DS, QSfw.saas-1DS and QSdw.saas-1DS explaining 7.92, 15.34, 9.64 and 10.15% of the phenotypic variation, respectively, were clustered in the region of 1DS from AX-94812958 to AX-110910133. Meanwhile, QPh.saas-7D, QTn.saas-7D, QSfw.saas-7D and QSdw.saas-7D were flanked by AX-109917900 and AX-110605376 on 7D, explaining 16.12, 24.35, 15.25 and 13.37% of the phenotypic variation on average, respectively. Moreover, these genomic QTLs on 1DS and 7D enhancing biomass in the parent Syn80 were from Ae. tauschii AT428. These findings suggest that these two QTLs from Ae. tauschii can be expressed stably in a hexaploid background at the jointing stage and be used for wheat improvement.

Introduction

Common wheat (Triticum aestivum L., 2n = 6x = 42, AABBDD), which is an important food crop throughout the world, originated from the spontaneous hybridization of tetraploid Triticum turgidum wheat (2n = 4x = 28, AABB) with diploid Aegilops tauschii Coss (2n = 2x = 14, DD) [1,2]. It is believed that only a few accessions of the donor species were involved in the evolution of common wheat, especially for the D genome donor. Consequently, the genetic diversity of common wheat decreased significantly compared to its donor species. Due to this evolutionary bottleneck, most of the genetic variation in Ae. tauschii did not exist in the commonly available hexaploid germplasm [3], and only 7% of the variants observed in Ae. tauschii were reserved in common wheat [4,5]. To enhance the transferal efficiency of elite genes from Ae. tauschii species to common wheat, scientists created synthetic hexaploid wheat (SHW) from crosses between T. turgidum and Ae. tauschii to broaden the genetic variation of hexaploid wheat [6]. Over 1000 SHW lines were produced by using more than 600 Ae. tauschii accessions stored at the International Maize and Wheat Improvement Center (CIMMYT; Mexico City, Mexico) [7]. SHWs with their vast genetic diversity have shown outstanding superiority in resistance to diseases and pests, tolerance to environmental stresses, and desirable quantitative traits, so these have been used widely in common wheat breeding [8–14]. Chinese scientists have shown a high interest in CIMMYT SHW lines since the early 1990s [15–18]. More than 200 CIMMYT SHW accessions were introduced into China in 1995 [14]. In recent years, several commercial wheat varieties have also been created and released in China [9,14,19]. In addition, several favourable introgressions from Ae. tauschii have been identified in synthetic derivatives [19]. A major QTL on 4DL associated with leaf sheath hairiness in a synthetic derivative of the wheat variety Chuanmai42 was identified, and its wild allele was found to have originated from Ae. tauschii, which has significantly increased grain weight, grain yield, and yield-related characters [20].

Vigorous cultivars have advantages for enhancing the population’s water-use efficiency by providing shade to the soil surface faster and thereby reducing evaporative losses from the soil [21–23]. Rapid early development of leaf area and the root system are associated with increased water and nutrient use efficiency, high rates of light interception and biomass production resulting in drought tolerance and high yield potential [22,23]. In recent years, we have screened CIMMYT SHWs for high biomass and found two SHWs (Syn79 and Syn80) derived from the same tetraploid wheat (durum wheat DOY1), with two different Ae. tauschii accessions, which have significantly different biomass during the entirety of the development stage. We attributed the significant difference in biomass between the two SHWs to the different genotypes in the two D genome donors. The vegetative growth, nutrient accumulation, nutrient distribution and utilization of Syn79 and Syn80 were significantly different under different environmental conditions [24]. To evaluate the genetic impact of the different D genomes on early vigour in hexaploid wheat, a population of recombinant inbred lines (RILs) derived from a cross between Syn79 and Syn80 was developed. The goal of this study was to map the major QTLs associated with early biomass accumulation contributed from Ae. tauschii in a hexaploid wheat background at jointing stage for the molecular breeding of wheat yield using SHWs.

Materials and methods https://dx.doi.org/10.17504/protocols.io.bgrnjv5e

Plant materials

Two hundred and three F₉ recombinant inbred lines (RILs) derived from a Syn79 x Syn80 cross and their parents were used for QTL mapping in this study. Syn79 and Syn80 were generated from durum wheat DOY1 (2n = 28, AABB) crossed with Ae. tauschii (2n = 14, DD) by CIMMYT [6]. A and B genomes of Syn79 and Syn80 were from the same durum donor DOY1, while their D genomes were from two different Ae. tauschii accessions (AT333 and AT428). Syn80 had stronger early vigour than Syn79 (Fig 1), due to their different D genomes, and AT428 possessed better early vigour traits than AT333.

Field trials

A total of five trials for Syn79, Syn80 and 203 RILs were conducted at Guang-Han Station (GHS) in 2017–2019 (2017GHS, 2018GHS, 2019GHS) and Cang-Shan Station (CSS) in 2017 and 2018 (2017CSS, 2018CSS). Both stations are members of the Sichuan Academy of Agricultural Sciences (SAAS). GHS and CSS are representative of the plains and hilly regions in Sichuan province, respectively. The chemical properties of the soil at these sites from five trials are shown in Table 1. The organic matter, total nitrogen and available nitrogen of the soil in GHS were all significantly higher than that in CCS, and the total potassium of the soil in CSS was more than that in GHS (Table 1).

Table 1. Chemical properties of soil in different field trials.

Trials	pH	Organic matter (g/kg)	Total nitrogen (g/kg)	Total phosphorus (g/kg)	Total potassium (g/kg)	Available nitrogen (mg/kg)	Available phosphorus (mg/kg)	Available potassium (mg/kg)
2017GHS	6.84	31.9	1.99	0.723	16.25	165	6.9	90
2018GHS	6.45	39.7	2.31	0.860	18.77	206	15.8	105
2019GHS	6.71	28.9	2.03	0.674	19.00	183	11.0	96
2017CSS	7.81	9.5	0.77	0.556	23.81	47	3.7	100
2018CSS	8.24	15.7	1.23	0.328	22.90	97	2.9	137

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The trials were performed in randomized complete blocks with three replicates. Each plot had five 1.5 m rows spaced 0.5 m apart. At the two-leaf stage, only ten evenly distributed plants in each row were retained for further growth. Field management consisted of commonly under-taken practices in wheat production.

Trait evaluation

Four early biomass related traits, plant height (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) per plant were investigated in the RILs and their parents at the jointing stage. The phenology and growing periods of the two parents and the RILs were only slight different, their phenotypic data were collected at one time when the first internode came out about 110 days after sowing. In each plot, 10 plants were randomly selected to evaluate traits associated with early biomass, dislodging plants at the ends of each row avoiding within-row edge effects. PH and TN were investigated in the field, which was finished within 1–2 days under the same trial environment. Then the shoots of these 10 sampled plants were cut for measuring SFW and SDW. SFW was accomplished within 12 hours after sampling. When measuring SDW, the separated shoot was dried to a constant weight at 65 °C after 10-minute exposure to 120 °C. All traits were described based on the mean values of 10 plants in each corresponding row.

SNP genotyping

A total of 50 mg of fresh plant leaves was collected from 2-week-old seedlings and DNA was extracted using the NuClean Plant Genomic DNA Kit (CWBio, Beijing, China). Eluted DNA was quantified using a Qubit 4 Fluorometer (Life Technologies Holdings Pte Ltd, Singapore) and then normalized using a 12-channel electronic pipette with a volume ranging from 10 to 100μL (Eppendorf, Hamburg, Germany) to obtain the concentration required for genotyping.

The RILs and their parents, Syn79 and Syn80, were genotyped on the Affymetrix platform of the Axiom Wheat Breeder’s Genotyping Array with 13947 SNP markers including 1272 functional markers by China Golden Marker Biotech Co Ltd (Beijing, China). The collected fluorescence signal from the SNP array processed and analyzed using functions in the apt-genotype-axiom for genotype calling, ps-metrics for generating various QC metrics and ps-classification for classifying SNPs in the software of Affymetrix Axiom Analysis Suite version 4.0.1. Among 13947 SNP markers, a total of 3480 SNPs were distributed on the D genome and were used for parental polymorphism analysis.

Statistical and QTL analysis

Descriptive analyses, analysis of variance (ANOVA) and correlation analyses for the phenotypic data were calculated using the SPSS statistical package (SPSS Inc., Chicago, IL). Variation of genotypes for phenotypic traits was evaluated using mean, standard deviation (SD), the coefficient of variation (CV), maximum (Max) and minimum (Min). An ANOVA was calculated for all traits based on a general linear model (GLM) to detect the effect of genotypes, environments and genotype × environment interactions. Broad sense heritability (H²) was estimated with the formula: H² = σ²g/ (σ²g + σ²ge/n + σ²e/nr), where σ²g is the genetic variance, σ²ge is the variance of the genotype-environment interaction, σ²e is the experimental error variance, n is the number of trials and r is the number of replications.

The QTL IciMapping Software version 4.1 [25,26] was used for genetic linkage map construction. The location of the SNP marker was aligned according to the physical map of Ae. tauschii AL8/78 for the D genome [27]. The genetic linkage map was constructed according to 153 polymorphic markers between Syn79 and Syn80 (the parents), which were screened from 3480 SNP markers distributed on the D genome. The map covered over 803.84 cM on the wheat D genome, with an average distance of 5.25 cM between adjacent polymorphic markers.

QTL analyses for the measured traits under the five different environmental conditions were performed using the inclusive composite interval mapping (ICIM) option on the QTL IciMapping Software version 4.1. The significant LOD threshold was determined by 1000 permutations and a significance threshold of P = 0.05. Linked QTLs with genetic distances of less than 20 cM were considered as one single QTL, which were named according to Ayalew et al. [28].

Results

Phenotypic analysis

Five different field trials were conducted at two locations over 3 years to evaluate early biomass related traits of the RIL population as well as their parents Syn79 and Syn80. Syn80 had greater early biomass than Syn79 (Fig 1). The values of PH, TN, SFW and SDW for Syn80 were significantly larger than those of Syn79 under all five environmental conditions (Table 2). Independent of the differences between the two parents, in all trials there was significant variation in the investigated traits of the RIL populations, with values spanning much larger ranges than those defined by the parental values. The phenotypic data were normally distributed in the RILs (Fig 2). Variation in the phenotypic data was tremendous in the RILs, especially for SFW and SDW. Variation was determined by genotype, environment and genotype × environment interactions. Their heritabilities ranged from 39.20 to 43.27% (Table 2). This suggested that those phenotypic traits were controlled by multiple genes and also significantly affected by the environment.

Table 2. Parental values, population distribution parameters, and heritability of the investigated traits.

Trait	Environment	Parents		RILs			H²	F-values from ANOVA
Trait	Environment	Syn79	Syn80	Mean±SD	CV(%)	Min-Max	(%)	Environment	Genotype	Environment×genotype
PH	2017GHS	31.87	48.64**	38.43±5.98	15.56	27.00–59.20	43.27	1368.74**	14.05**	2.02**
(cm)	2018GHS	34.48	53.81**	50.12±8.07	16.10	29.38–65.33
	2019GHS	46.11	63.33**	60.87±8.20	13.47	38.11–81.94
	2017CSS	42.00	56.33**	54.40±8.34	15.33	27.17–69.33
	2018CSS	49.67	65.11**	59.84±9.07	15.16	27.58–76.56
TN	2017GHS	5.60	12.53**	10.01±2.58	25.77	4.50–17.90	43.11	780.24**	14.32**	2.05**
(No./plant)	2018GHS	8.17	16.67**	15.05±3.92	26.05	6.00–23.00
	2019GHS	10.00	15.78**	14.23±3.73	26.21	5.78–21.67
	2017CSS	7.00	12.00**	9.22±2.58	27.98	2.00–15.00
	2018CSS	8.33	13.22**	11.16±3.31	29.66	2.33–18.33
SFW	2017GHS	17.09	73.72**	48.25±25.60	53.06	7.02–136.54	40.20	144.40**	14.05**	2.16**
(g/plant)	2018GHS	21.79	70.78**	60.92±29.91	49.10	7.30–156.94
	2019GHS	29.40	78.37**	64.94±29.89	46.03	10.97–169.70
	2017CSS	26.58	82.57**	52.69±25.50	48.40	3.59–132.55
	2018CSS	36.89	96.08**	75.44±39.27	52.05	4.72–158.86
SDW	2017GHS	2.85	10.22**	6.64±3.34	50.30	1.04–16.19	39.20	161.47**	84.08**	6.60**
(g/plant)	2018GHS	3.43	10.24**	8.35±3.58	42.87	1.04–20.54
	2019GHS	4.63	11.87**	8.96±4.31	48.10	1.43–17.80
	2017CSS	4.43	11.45**	7.25±3.28	45.24	0.46–18.13
	2018CSS	5.59	13.98**	10.18±4.95	48.62	0.69–20.57

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* And ** indicate significant differences at P = 0.05 and 0.01, respectively. PH: plant height, TN: tiller number, SFW: shoot fresh weight, SDW: shoot dry weight, SD: standard deviation, CV: the coefficient of variation, Max: maximum, Min: minimum, RILs: recombinant inbred lines, H²: broad sense heritability, ANOVA: analysis of variance.

Correlations among PH, TN, SFW and SDW in each trial are presented in Table 3. This shows that significant positive correlations among these traits were detected in the early growth stage. The average coefficients in the five trials ranged from 0.581 to 0.975. PH was significantly positively correlated with TN, and the coefficients ranged from 0.424 to 0.683 across each trial (Table 3). Both PH and TN showed significant positive correlations with SFW and SDW, and the coefficients were higher than that between PH and TN. These results suggest that greater early biomass is related with higher PH, more TN, heavier SFW and SDW.

Table 3. Correlation coefficients between the four traits in RILs in different trials.

	TN	SFW	SDW
PH	0.673**	0.724**	0.733**
	0.424**	0.364**	0.355**
	0.683**	0.784**	0.808**
	0.606**	0.821**	0.835**
	0.612**	0.791**	0.791**
TN		0.708**	0.711**
		0.142*	0.141*
		0.731**	0.728**
		0.668**	0.678**
		0.749**	0.713**
SFW			0.967**
			0.969**
			0.978**
			0.983**
			0.980**

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*And** indicate significance at P = 0.05 and 0.01 level, respectively. PH: plant height, TN: tiller number, SFW: shoot fresh weight, SDW: shoot dry weight.

Genetic map of the D genome

In this study, we used a Wheat Breeder’s Genotyping Array to genotype the A, B and D genomes. For the A and B genomes, a total of 10467 SNP labels anchored on the genotyping array were used to check the genotype of the A and B genomes in the RIL population and their parents, which were generated from the same A and B genomes’donor. The results showed that almost all SNP markers on the A and B genomes had no polymorphism between the two parents. For the D genome, 3480 SNP labels were selected to fix on the chip by China Golden Marker Biotech Co Ltd (Beijing, China). Among these scanned markers, 153 markers on the D genome had polymorphism between the two parents, which were unequally distributed on the seven chromosomes of the D genome (Table 4). The number of polymorphic markers on different chromosomes ranged from 8 on 3D to 34 on 7D (Table 4).

Table 4. SNP markers on the D genome.

Parameter	1D	2D	3D	4D	5D	6D	7D	Total
Total Makers	370	634	536	265	550	428	697	3480
Polymorphic markers	30	20	8	21	25	15	34	153
Polymorphism rate (%)	8.11	3.15	1.49	7.92	4.55	3.50	4.88	4.40
Map length (cM)	127.58	69.22	21.35	145.52	135.72	89.95	214.50	803.84
Distance between polymorphic markers (cM)	4.25	3.46	2.67	6.93	5.43	6.00	6.31	5.25

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For linkage map construction, SNP markers were grouped according to their anchored chromosomes in the Ae. tauschii AL8/78 D genome, and then aligned by the nnTwoOpt method [25–27]. The entire genetic map covered over 803.84 cM of the D genome with an average distance between adjacent markers of 5.25 cM (Table 4). The average distance between two adjacent markers ranged from 2.67 cM to 6.93 cM. For all of the 7 chromosomes, the linkage maps ranged from 21.35 cM to 214.50 cM. For the chromosomes 2D and 3D, the total distances of the constructed linkage maps in this population and the Wheat Breeder’s Genotyping Array were 69.22 cM and 21.35 cM, respectively. Out of the genomic regions of the linkage maps, no polymorphic markers were detected by this SNP array.

Genotypic markers were tested for segregation distortion (deviation from the expected 1:1 ratio) by Chi-squared tests. Among the 153 SNP loci, 54 loci showed segregation distortion in RILs (Table 5). Almost all loci were biased to Syn80, showing larger early biomass, which means that in those loci most of the progeny RILs preferentially inherited the female parent Syn80. Only four loci were male-biased (Table 5). Among those female-biased loci, the number of loci on the different chromosomes were distributed from 1 on 3D to 18 on 7D. Three genomic regions were detected as Syn80-biased on chromosome 1D, 2D and 7D (Table 5), and these covered about 50, 20 and 40 cM on 1D, 2D and 7D, respectively.

Table 5. Segregation distortion of SNP loci in RILs.

Chromosome	Syn80-biased Locus		Unbiased Locus		Syn79-biased Locus
Chromosome	Number	Rate (%)	Number	Rate (%)	Number	Rate (%)
1D	11	36.67	19	63.33	0	0.00
2D	14	70.00	5	25.00	1	5.00
3D	1	12.50	7	87.50	0	0.00
4D	2	9.52	19	90.48	0	0.00
5D	3	12.00	20	80.00	2	8.00
6D	1	6.67	14	93.33	0	0.00
7D	18	52.94	15	44.12	1	2.94
Total	50	32.68	99	64.71	4	2.61

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Underline means genetic regions with linked loci; Chi-squared tests were considered at the P = 0.05 level

QTLs on the D genome

With the linkage map constructed by 153 SNP markers on the D genome, QTLs for PH, TN, SFW and SDW were identified under five environmental conditions using the inclusive composite interval mapping program (ICIM).

PH and TN are common agronomic traits in wheat, and the higher PH and TN in the seedling growth stage were positively correlated with the enhanced water-use efficiency of the population due to the soil surface being shading faster, which reduces evaporative losses from the soil. A total of two QTLs for PH were identified on chromosome 1DS and 7D (Table 6; Fig 3). The QTL peak of the first one was located in the interval of AX-94812958 and AX-110910133 under multiple environmental conditions, and its physical position was located on the genomic interval of 8.97–21.51 Mb according to the sequence assembly of Ae. tauschii AL8/78 [27]. Under the five environmental conditions, this QTL explained 6.91–9.17% of the phenotypic variation (PVE). And the QTL allele from Syn80 increased the PH of seedlings, with its additive effect ranging from 1.93 to 2.92 cm (Table 6). The second QTL was located in the interval of AX-109917900—AX-110605376 with its physical interval corresponding to 324.36–557.58 Mb in Ae. tauschii AL8/78. QPh.saas-7D explained an average PVE of 16.12% across the different environments. Seedling height on the QTL allele from the parent Syn80 increased more than 5 cm in the trial of 2019GHS (Table 6). For TN, two QTLs, QTn.saas-1DS and QTn.saas-7D were detected under all five environmental conditions (Table 6; Fig 3). Their intervals were in accordance with the PH QTLs on chromosome 1DS and 7D, respectively (Table 6; Fig 3). The PVE of QTn.saas-1DS ranged from 6.32% to 19.55% with an average of 15.34%, and was able to increase the tiller number by about 2 tillers from Syn80 in the trial of 2018GHS (Table 6).

Table 6. QTLs for plant weight (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) in the RILs.

Traits	QTL	Environments	Peak position (cM)	Marker interval	Physical interval (Mb)	LOD	PVE (%)	ADD^¶
PH	QPh.saas-1DS	2017GHS	1DS:34	AX-94812958 ^a - AX-109908110 ^b	8.97–11.57	4.87	9.17	-1.93
		2018GHS	1DS:34	AX-94812958 - AX-109908110	8.97–11.57	4.49	8.15	-2.58
		2019GHS	1DS:34	AX-94812958 - AX-109908110	8.97–11.57	4.86	6.91	-2.31
		2017CSS	1DS:40	AX-94812958 - AX-110910133 ^c	8.97–21.51	2.90	7.71	-2.92
		2018CSS	1DS:39	AX-94812958 - AX-110910133	8.97–21.51	2.90	7.68	-2.60
	QPh.saas-7D	2017GHS	7D:90	AX-109917900 ^d - AX-110605376 ^e	324.36–557.58	7.81	14.64	-2.51
		2018GHS	7D:91	AX-109937582 ^f - AX-110605376	549.19–557.58	6.87	12.86	-3.33
		2019GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	20.16	34.33	-5.35
		2017CSS	7D:90	AX-109917900 - AX-110605376	324.36–557.58	4.08	9.00	-2.75
		2018CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	5.98	9.77	-3.31
TN	QTn.saas-1DS	2017GHS	1DS:33	AX-94812958 - AX-109908110	8.97–11.57	3.36	6.32	-0.73
		2018GHS	1DS:37	AX-94812958 - AX-110910133	8.97–21.51	8.82	16.34	-1.82
		2019GHS	1DS:34	AX-94812958 - AX-109908110	8.97–11.57	12.39	15.54	-1.54
		2017CSS	1DS:38	AX-94812958 - AX-110910133	8.97–21.51	10.26	19.55	-1.32
		2018CSS	1DS:35	AX-94812958 - AX-110910133	8.97–21.51	12.93	18.93	-1.42
	QTn.saas-7D	2017GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	8.38	16.68	-1.24
		2018GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	12.29	18.88	-2.12
		2019GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	26.15	38.25	-2.52
		2017CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	13.51	19.27	-1.46
		2018CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	19.48	28.66	-1.86
SFW	QSfw.saas-1DS	2017GHS	1DS:33	AX-94812958 - AX-109908110	8.97–11.57	3.70	7.51	-8.98
		2018GHS	1DS:34	AX-94812958 - AX-109908110	8.97–11.57	6.40	11.31	-11.17
		2019GHS	1DS:36	AX-94812958 - AX-110910133	8.97–21.51	7.23	12.63	-10.11
		2017CSS	1DS:42	AX-94812958 - AX-110910133	8.97–21.51	2.96	8.03	-8.26
		2018CSS	1DS:36	AX-94812958 - AX-110910133	8.97–21.51	4.27	8.71	-10.30
	QSfw.saas-7D	2017GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	4.83	9.13	-10.13
		2018GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	9.07	16.25	-13.70
		2019GHS	7D: 91	AX-109937582 - AX-110605376	549.19–557.58	15.97	26.61	-15.88
		2017CSS	7D: 91	AX-109937582 - AX-110605376	549.19–557.58	6.03	10.17	-10.93
		2018CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	7.66	14.08	-14.22
SDW	QSdw.saas-1DS	2017GHS	1DS:40	AX-94812958 - AX-110910133	8.97–21.51	4.35	10.59	-1.39
		2018GHS	1DS:34	AX-94812958 - AX-109908110	8.97–11.57	6.93	12.28	-1.53
		2019GHS	1DS:36	AX-94812958 - AX-110910133	8.97–21.51	6.98	12.84	-1.40
		2017CSS	1DS:40	AX-94812958 - AX-110910133	8.97–21.51	2.73	7.24	-1.02
		2018CSS	1DS:35	AX-94812958 - AX-110910133	8.97–21.51	3.93	7.79	-1.28
	QSdw.saas-7D	2017GHS	7D:89	AX-109917900 - AX-110605376	324.36–557.58	4.40	6.53	-1.22
		2018GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	8.24	14.81	-1.71
		2019GHS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	13.10	22.20	-2.00
		2017CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	5.77	10.09	-1.38
		2018CSS	7D:91	AX-109937582 - AX-110605376	549.19–557.58	6.88	13.24	-1.76

Open in a new tab

^{a, b, c, d, e, f} indicate the Chi-square value = 38.506 (P<0.001), 57.346 (P<0.001), 6.821 (P<0.01), 76.722 (P<0.001), 79.258 (P<0.001) and 82.713 (P<0.001) for segregation distortion at these markers, respectively.

^¶Additive effect. Positive, negative mean Syn79, Syn80 alleles produced larger values, respectively. PH: plant height, TN: tiller number, SFW; shoot fresh weight, SDW: shoot dry weight

SDW is positively related to SFW at the seedling stage. In this study, we detected two QTLs for both SFW and SDW on the chromosome 1DS and 7D (Table 6; Fig 3). The QTL intervals for SFW and SDW were in accordance with the QTL intervals for both PH and TN. Since higher plant height and a greater tiller number per plant resulted in larger SFW and SDW, this suggests that these may be the same QTLs. The average PVE for QSfw.saas-1DS and QSdw.saas-1DS was 9.64% and 10.15%, respectively. The QTL allele from Syn80 increased the SFW and SDW (Table 6). In the interval of AX-109937582—AX-110605376 on chromosome 7D, QTLs for both SFW and SDW were identified under all five environmental conditions, and the average PVE of QSfw.saas-7D and QSdw.saas-7D was 15.25% and 13.37%, respectively (Table 6). The QTL alleles that increased SFW and SDW were from the parent Syn80 (Table 6).

In this study, two genomic regions were identified to be associated with early biomass. They were in the interval of AX-94812958—AX-110910133 on chromosome 1DS and the interval of AX-109917900—AX-110605376 on chromosome 7D. The two genomic regions from the parent Syn80 could significantly enhance the early biomass with pleiotropic effects of increasing PH, TN, SFW and SDW.

Discussion

Greater early biomass is visual and important for breeding new varieties and innovative utilization of crop germplasm, especially under adverse environmental conditions. Therefore, it is important to select traits under drought stress [29–31], especially in Sichuan, where drought or seasonal drought occurred frequently in the last 70 years [32]. In this study, the early biomass of the parents and the RIL population showed significant phenotypic differences in PH, TN, SFW and SDW under the five different environmental conditions from 2016 to 2019. Phenotypic and QTL analyses demonstrated that the early biomass related traits, PH, TN, SFW and SDW, were controlled by polygenes. Wheat growth habit types (spring or winter), the wheat growth progress and early biomass were affected by the combination of photoperiod and vernalization genes [33–36]. Photoperiod and vernalization genes on the D genome were located on 2D and 5D [33,34]. Considering that the phenology and growing periods of the two parents and the RILs were slight different, it can be inferred that early biomass in these RILs was controlled by genes, which could not be related to photoperiod or vernalization genes, for no QTLs were detected on the chromosomes 2D or 5D.

In the present study, two synthetic wheat varieties, Syn79 and Syn80, were generated from two different Ae. tauschii accessions crossed with the same tetraploid wheat, and the significant difference in early biomass between them was caused by their different D genome donors. Ae. tauschii, the D genome donor of common wheat, exhibited genetic diversity for early growth and might be a valuable species for improvement of early vigour in wheat [37]. The common wheat D genome progenitor, Ae. tauschii, showed a rapid leaf expansion rate at the seedling stage [21,37], which is beneficial for reducing evaporative losses from the soil [21]. Genetic dissection for early vigour related traits has been reported in several germplasms under different growing conditions, and QTLs for early vigour related traits were distributed through almost the whole genome of the wheat [21,37–41]. ter Steege et al identified 87 QTLs for early growth that were related to 33 traits, 3.1 QTLs per trait, explaining 32% of the PVE by using a population of Ae. tauschii RILs at the seedling stage, but there was no significant QTLs for plant and shoot mass detected in this study, considering that the effects of QTL for the underlying growth traits counterbalanced each other [37]. However, in our study, two chromosome fragments for SFW and SDW were detected, which simultaneously regulated PH and TN. The favorable alleles detected were from Ae. tauschii and they could express stably in a hexaploid genetic background. Few QTLs for biomass have been identified in the diploid populations of Ae. tauschii [37], but in a hexaploidy genetic background. In the present study these expressed stably in synthetic hexaploid wheat. The AABB genome of tetraploid wheat may play a very important role in synthetic wheat derived from crosses of tetraploid wheat and Ae. tauschii. The effects of genome combination between AABB and DD for gene expression need to be analyzed further. And it substantiates the conclusion that using SHW is a more effective method to transfer favourable genes from Ae. tauschii to common wheat [6,7,9,42].

In addition, the two chromosome fragments for PH, TN, SFW and SDW were detected stably on 1DS and 7D, which were located on the genomic intervals of 8.98–21.51 Mb and 324.36–557.58 Mb, respectively. Lr42, Rmg6, Sr33, SrTA1662, LR10, Xa5, Chalk5, MHZ5, B10, Rc, BC10, EBR1 and EBR1 were located in the interval of AX-94812958 -AX-110910133 on 1DS of Ae. tauschii, and 16 QTL/genes (Pid2, IPA1, Xa13, Hd18, GW8, Xa27-Xa27-IRBB27, qUVR-10, Yr33, Dn2, Ehd3, Nud, OsABCG15, MOC1, Lks2, TaD27 and QTls for antixenosis) were in the interval of AX-109917900 -AX-110605376 on 7D [43]. Among these reported genes, none except for TaD27 on 7D, which was associated with tiller number in hexaploidy, has been found to be related to early vigour previously.

Segregation distortion is a common phenomenon among many plants [44]. In the present study, 54 of 153 SNP loci showed segregation distortion in the RILs, and 50 makers were skewed to Syn80, while 4 were biased to Syn79. Segregation distortion loci accounted for 35.29% of the total polymorphic loci, and 92.59% of the loci were preferentially biased to the female parent Syn80, with only 7.41% coming from male parent Syn79. At the same time, we found that Syn80 had stronger seedling vigour than that of Syn79. Therefore, the early vigour which afforded a high survival ratio in the RILs containing the Syn80 loci, was higher than that of the RILs containing the Syn79 loci. The proportion of segregation distortion was high in the RILs. Xu et al found a similar phenomenon, finding that the purer the population, the higher separation ratio [45]. In the present study, three genomic regions were detected to be Syn80-biased on chromosome 1D, 2D and 7D (Table 5), which were involved with the QTL intervals for early biomass. The centre of segregation bias on chromosome 1DS was located in the interval of AX-110090502—AX-109911195 with a genetic location from 8.26 cM to 12.44 cM, as 96.4% of the progeny shared the same genotype with the parent Syn80 at the SNP site of AX-110090502 and 97.9% for AX-109911195. On chromosome 2D, the segregation bias region was framed from AX-108911375 to AX-110935958 across about 20 cM. On 7D, the centre of segregation bias was located in the interval of AX-110271371 to AX-94807766. The centre of segregation bias on 1DS was about 25 cM away from the detected QTL peaks for early growth-related traits, and the centre of segregation bias on 7D was located in the interval of the QTL peaks detected on this chromosome. Many factors may cause segregation distortion, these can be genetic factors such as reproductive isolation, or incoordination between the cytoplasm and nucleus, or hybrid necrosis etc. [46], and these can be due to natural or artificial selection [47]. In most cases, segregation is controlled by reproductive isolation factors such as gametophyte genes on the nucleus or sterility genes [48–51]. Several types of hybrid abnormalities including hybrid necrosis were reported in the process of synthetic wheat production [52,53]. Usually, these abnormal growth phenotypes are classified into hybrid necrosis (Types II and III), hybrid chlorosis and severe growth abortion [54,55]. Two genes derived from Ae.tauschii related to type II and III necrosis symptoms have been mapped [53,54]. The gene Nec1 of type III necrosis was on chromosome 7DS [54], while the gene Nec2 of type II necrosis was on chromosome 2DL [56]. The locations of Nec2 and Nec1 were close to the segregation bias region on chromosome 2D and the segregation bias centre on chromosome 7D. One possible reason for the segregation bias for Syn80 in these loci was that Syn79 may have carried the Nec2 and Nec1 alleles for hybrid necrosis. Thus, the segregation bias would have spread from the location of Nec2 or Nec1 across the QTL regions in this population. Segregation distortion regions may be related to certain genes, the gene location of the target trait can be preliminarily determined according to the segregation distortion region of the genetic map and the phenotypic data. However, no strong evidence showed that the early biomass QTL was caused by the segregation bias to Syn80.

In the present study, 3480 SNP markers were used on the D genome, and only 153 polymorphic markers were detected between the parents, a percentage polymorphism of 4.40%. Comparing to the genetic diversity of Ae. taushcii and the wheat cultivars reported by previous authors [56–58], Syn79 and Syn80 had low genetic diversity on the D genome. It has been widely accepted that Ae. tauschii ssp. strangulata is the D genome donor of hexaploid wheat [56,59–63]. Ae. tauschii was classified into two groups, lineage 1 and lineage 2 [56,64]. Lineage 1 is broadly related to Ae. tauschii ssp. tauschii and lineage 2 is broadly related to Ae. tauschii ssp. strangulata. The Infinium SNP array for the D genome was developed mainly according to the SNP polymorphism between Ae. tauschii ssp. tauschii and Ae. tauschii ssp. strangulata. Therefore, the D genome donors (AT333 and AT428) of synthetic hexaploid wheat Syn79 and Syn80 may belong to the same group (Lineage 1 or Lineage 2), and their genetic relationship is very close. Although the number of polymorphic loci in the D genome between Syn79 and Syn80 was low, two genome regions on 1DS and 7D for four early biomass related traits were still detected under five different environmental conditions. This provided a basis for further fine mapping and candidate gene analysis of a few QTLs for early biomass related traits. On the other hand, each of the synthetic wheat Syn79 and Syn80 combining elite genes from tetraploid wheat and Ae. tauschii is a potential resource to broaden the genetic diversity for wheat breeding programs.

Conclusion

By using a set of recombinant inbred lines derived from two synthetic hexaploid wheat varieties (Syn79 and Syn80) re-synthesized from the same tetraploid wheat DOY1 and two different Ae. tauschii accessions (AT333 and AT428), two genomic regions on 1DS and 7D were detected to be associated with early biomass, with pleiotropic effects on PH, TN, SFW and SDW. The QTL alleles from Syn80 enhanced the early biomass by increasing PH, TN, SFW and SDW, and these originated from the Ae. tauschii AT428, which expresses stably in a hexaploid background. The framed SNP markers could be used for wheat improvement.

Supporting information

S1 Data

(XLS)

Click here for additional data file.^{(450KB, xls)}

S2 Data

(XLS)

Click here for additional data file.^{(244.5KB, xls)}

S3 Data

(XLS)

Click here for additional data file.^{(39KB, xls)}

Acknowledgments

We thank the International Maize and Wheat Improvement Center for providing synthetic hexaploid wheat parents (Syn79 and Syn80). The National Natural Science Foundation of China and the Department of Science and Technology of Sichuan Province supported this work. We also thank our colleagues and staff at the Guang-Han Station and the Cang-shan Station of the Sichuan Academy of Agricultural Sciences for their helps in this study.

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

This work was financially supported by National Natural Science Foundation of China (Grant No. 31661143007, 31401383) and Department of Science and Technology of Sichuan Province (Grant No. 2017JY0077, 2017JY0286, 2020YJ0469).

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64.Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S. Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol. 2010; 19: 999–1013. 10.1111/j.1365-294X.2010.04537.x [DOI] [PubMed] [Google Scholar]

PLoS One. doi: 10.1371/journal.pone.0234882.r001

Decision Letter 0

Aimin Zhang

13 Mar 2020

PONE-D-20-04315

Mapping QTL for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

PLOS ONE

Dear Dr Yang,

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PLOS ONE

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Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This manuscript described analysis of QTLs related to early biomass using a RIL population derived from two synthetic hexaploid wheat with same AABB-genome background. Four stable QTL for plant height (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) were detected on chromosomes 1D and 7D. The manuscript presented some interesting results using synthetic hexaploid wheat accessions distinguished by only D genome. I felt this manuscript is valuable because that diversity of wheat D genome is very low. The introduction of novel D-derived genes through synthetic hexaploid is a efficient way to expand genetic background of bread wheat. The identification of novel QTLs for early biomass from Aegilops tauschii are valuable for wheat improvement. It will be of interest for the readers of Plos one. Thus, this manuscript is acceptable, but there are some problem needs to be addressed.

1)There are some witting errors needs thorough correction, some were marked on the pdf. And the language also need improve.

2)Some statistical information need to reconfirm and replenish.

P10-L181-183: The authors claim that the H2 =0.4327 for PH is significant lower than the results of previous reported. I suggested that the authors perform an ANOVA again to confirm whether the error variance is too large or the calculation is wrong.

P13-L221-228.: The genetic map constructed in present study containing 54 segregation distortion loci. I suggested that the authors confirm whether these segregation distortion loci have an effect on QTL mapping.

P19-L290-293: The authors claim that the growing periods of two parents and RILs were consistent, but I found this claim was not supported by the presented data.

Reviewer #2: This manuscript reports important chromosomal positions of QTLs for four biomass traits that affect wheat yield and tolerance to abiotic stresses. It would be worthy of being published if the numerous typographical and grammatical errors (identified in the uploaded file) are corrected throughout the manuscript. It is also suggested that authors modify the figure of chromosomes 1D and 7D to depict the centromeres.

**********

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Reviewer #1: No

Reviewer #2: Yes: Richard R.-C. Wang

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Attachment

Submitted filename: PONE-D-20-04315_reviewer.pdf

Click here for additional data file.^{(1.1MB, pdf)}

Attachment

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Click here for additional data file.^{(683.3KB, docx)}

PLoS One. 2020 Jun 25;15(6):e0234882. doi: 10.1371/journal.pone.0234882.r002

Author response to Decision Letter 0

31 Mar 2020

Thank you very much for giving us an opportunity to revise our manuscript, we appreciate editor and reviewers very much for their positive and constructive comments and suggestions on our manuscript. We have accepted all the modifications made by the two reviewers, and answered the comments carefully. We have tried our best to revise our manuscript according to the reviewers’ comments and PLOS ONE’s style requirements. In addition, this manuscript was edited for proper English language, grammar, punctuation, spelling, and overall style by one or more of the highly qualified native English speaking editors at NativeEE. We have made revision which marked in red in the paper.

Point-to-point reply:

1) Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

Response:

Thanks for your reminder. We carefully have read PLOS ONE’s style requirements again, and carefully modified to meet its style requirements.

2) We suggest you thoroughly copyedit your manuscript for language usage, spelling, and grammar.

Response:

Thanks for your suggestion. Native English speaking editors at Native English Editing checked and corrected for English language, spelling, grammar.

Upon resubmission, please provide the following:

�The name of the colleague or the details of the professional service that edited your manuscript

�A copy of your manuscript showing your changes by either highlighting them or using track changes (uploaded as a *supporting information* file)

�A clean copy of the edited manuscript (uploaded as the new *manuscript* file)

Response:

OK. We will resubmit the manuscript according to your requirements.

Our manuscript for language usage, spelling, and grammar were checked and corrected by native English speaking editors at Native English Editing, which provided a statement of editing. We uploaded as separate file and labeled ‘Statement of Editing’.

We showed our changes in our manuscript by in red font. The file was uploaded separately and labeled ‘Revised Manuscript with Track Changes’.

We uploaded a clean manuscript separately, this file was labeled ‘Manuscript’.

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Response:

OK. The corresponding author Wuyun Yang has an ORCID iD, and it is validated in Editorial Manager.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #2: Yes

Response:

Thanks for your recognition.

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

Response:

Thanks for your recognition.

3.Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #2: Yes

Response:

Thanks for your recognition.

4. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #2: No

Response:

We have tried our best to modify the manuscript. At the same time, this manuscript was edited for proper English language, grammar, punctuation, spelling, and overall style by one or more of the highly qualified native English speaking editors at NativeEE. We hope that the revised manuscript can meet PLOS ONE’s requirements.

5. Review Comments to the Author

Reviewer #1: This manuscript described analysis of QTLs related to early biomass using a RIL population derived from two synthetic hexaploid wheat with same AABB-genome background. Four stable QTL for plant height (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) were detected on chromosomes 1D and 7D. The manuscript presented some interesting results using synthetic hexaploid wheat accessions distinguished by only D genome. I felt this manuscript is valuable because that diversity of wheat D genome is very low. The introduction of novel D-derived genes through synthetic hexaploid is a efficient way to expand genetic background of bread wheat. The identification of novel QTLs for early biomass from Aegilops tauschii are valuable for wheat improvement. It will be of interest for the readers of Plos One. Thus, this manuscript is acceptable, but there are some problem needs to be addressed.

1)There are some witting errors needs thorough correction, some were marked on the pdf. And the language also need improve.

Response:

Thank you for your careful revision. We have accepted your correction. We have tried our best to modify the manuscript. At the same time, this manuscript was edited for proper English language, grammar, punctuation, spelling, and overall style by one or more of the highly qualified native English speaking editors at NativeEE. We hope that the revised manuscript can meet PLOS ONE’s requirements.

2)Some statistical information need to reconfirm and replenish.

Response:

In this study, the PH was investigated at the jointing stage. The method of measuring PH was different from the measure of PH in the mature period, which is the length of the main stem, measured from ground level to the tip of spike, excluding awns. However, the PH of seedling in this study was measured from ground level to the tip of the first leaf. We infer that the lower H2 for PH in this study was caused by the alterable length of the first leaf, as H2 for the length of wheat leaf was much lower that the PH in the mature period. Actually, it is hard to investigated the plant height before heading time.

Plant height is a complex trait, and is controlled by multiple major genes and micromajor genes. The QTLs detected in our research were micromajor genes, their heritability was lower, compared to the major genes.

We performed an ANOVA again, as was shown in table 1 below. The ANOVA results showed that variation of plant height was determined by genotype, environment and genotype × environment interactions (Table 2 in manuscript). Anyway, the lower H2 for PH in this study could be considered to be caused by the multi-environments.

Table 1 - ANOVA analysis of RIL population in five different field environments.

Trait Sum of squares df Mean square F Sig.

Environment PH(cm) 156917.231 4 39229.308 1368.743 .000

TN(No./plant) 15260.574 4 3815.143 780.237 .000

SFW(g/plant) 249927.824 4 62481.956 144.401 .000

SDW(g/plant) 4629.493 4 1157.373 161.466 .000

Genotype PH(cm) 81328.358 202 402.616 14.048 .000

TN(No./plant) 14145.042 202 70.025 14.321 .000

SFW(g/plant) 1227777.367 202 6078.106 14.047 .000

SDW(g/plant) 121740.517 202 602.676 84.080 .000

Environment×genotype PH(cm) 46743.096 808 57.850 2.018 .000

TN(No./plant) 8113.498 808 10.041 2.054 .000

SFW(g/plant) 756089.686 808 935.755 2.163 .000

SDW(g/plant) 38235.366 808 47.321 6.602 .000

Error PH(cm) 52363.345 1827 28.661

TN(No./plant) 8933.524 1827 4.890

SFW(g/plant) 790535.902 1827 432.696

SDW(g/plant) 13095.739 1827 7.168

Total PH(cm) 8540199.707 2842

TN(No./plant) 460303.452 2842

SFW(g/plant) 13613684.720 2842

SDW(g/plant) 357908.221 2842

Response:

In this study, 54 segregation distortion loci were detected, but these segregation distortion loci don’t affect QTL mapping. If the high density map was constructed accurately, and then the impact of segregation distortion on QTL analysis can be ignored. QTL IciMapping software can be used to construct genetic map, QTL mapping in segregation distortion population. And we checked the segregation ratio of the loci framed the QTLs and no significant segregation distortion was found. And the relevant results were described in the discussion of the manuscript (P21-L343-346 ans P22-L361-364).

P19-L290-293: The authors claim that the growing periods of two parents and RILs were consistent, but I found this claim was not supported by the presented data.

Response:

Sorry, the expression of this sentence is not accurate enough. Actually, the difference of growing periods between two parents and RILs exist, but was very small. And we revised the sentence, changed ‘consistent’ into ‘slight different’.

Response:

Thank you for your careful revision, suggestion on our manuscript, and recognition of our work. We have accepted your correction. We have tried our best to modify the manuscript. At the same time, this manuscript was edited for proper English language, grammar, punctuation, spelling, and overall style by one or more of the highly qualified native English speaking editors at NativeEE.

We have modified the figure of 1D and 7D, and attached the position of the centromeres (Fig 3).

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Richard R.-C. Wang

Response:

Yumin Yang register a user(362072749@qq.com), and upload our the three figure files, they are valid TIF files.

Response to comments in manuscript by reviewer #1：

1.P9-L169-L171：”Independent of the differences between the two parents, in all trials there were significant variations in the investigated traits of the RIL populations, with values spanning much larger ranges than those defined by the parental values.” This sentence is little confusing.

Response:

We want to state the transgressive inheritance. so we added it to avoid confusion (P9-L171-L174).

2. P13-L212:”and then aligned by nnTwoOpt method.” ref should be added.

Response:

This sentence’s ref were added (P13-L214).

3.P20-L310：”Few QTLs for biomass have been identified in the diploid populations directly from Ae. tauschii, but in a hexaploidy genetic background.”

results or refs supporting this should be added.

Response:

We want to state that ter Steege et al haven’t detected QTLs for biomass in diploid populations of Ae. tauschii, but we detected in synthetic hexaploid wheat. This sentence added ref, and the sentence changed into “Few QTLs for biomass have been identified in the diploid populations of Ae. tauschii [37], but in a hexaploidy genetic background.”(P20-L313-L315).

Response to comments in manuscript by reviewer #2：

1. P7-L133-L135:The RILs and their parents Syn79 and Syn80 were executed on the Affymetrix platform of Axiom Wheat Breeder’s Genotyping Array with 13947 SNP markers including 1272 functional markers by China Golden Marker Biotech Co Ltd (Beijing, China).

“executed” need a better word.

Response:

We changed “executed” into “genotyped” (P7-L134)

2. P23-L380-L382: On the other hand, each of the synthetic wheat Syn79 and Syn80 having newly genes from tetraploid wheat and Ae. tauschii is a potential resource to broaden the genetic diversity for wheat breeding programs.

Newly acquired? Any evidence for the newly acquired genes in SHWs resulted from gene recombination following hybridization of tetraploid wheat and Ae. tauschii?

Response:

Sorry, the expression of “newly genes’ is not accurate enough, because we have no relevant evidence to confirm whether these genes have been reported. We can make sure that Syn80 has QTLs for enhancing early biomass in this study, with pleiotropic effects on plant height, tiller number, shoot fresh weight and shoot dry weight. These genes were elite genes from tetraploid wheat and Ae. tauschii. So we revised this sentence, and changed ‘newly genes’ into ‘ combining elite genes’ (P23-L386).

Attachment

Submitted filename: Response to Reviewers.doc

Click here for additional data file.^{(109KB, doc)}

PLoS One. doi: 10.1371/journal.pone.0234882.r003

Decision Letter 1

Aimin Zhang

30 Apr 2020

PONE-D-20-04315R1

Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

PLOS ONE

Dear Dr Yang,

We would appreciate receiving your revised manuscript by Jun 14 2020 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Aimin Zhang, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #3: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #3: No

**********

6. Review Comments to the Author

Reviewer #1: As all questions have been addressed, I felt that this manuscript could be accepted for publication.

Reviewer #3: This paper described the mapping studies of QTLs related to early biomass using a RIL population derived from two synthetic hexaploid accessions with the same tetraploid background. Two major QTLs for four biomass related traits were detected on chromosomes 1DS and 7D. The data was interesting and should provide us with useful information on expanding the diversity of wheat D genome. However, a minor revision is needed for publication.

Some points are:

1. The growing periods of RILs were the controlling factors for precise evaluation of the biomass related phenotypes, because the jointing stage was a relatively broad description. Please clarify it in M & M, for example, how many days after sowing to start phenotype evaluation, and how many days needed for finishing the plant height and tiller number evaluation and sampling for all the RILs?

2. About the loci with segregation distortion. Please add the Chi-squared test of the most significant SNPs for each QTL in Table 6.

3. The language also need to be improved, for example, in line 43, change ‘the QTLs’ to ‘these two QTLs’; line 171, ‘There was transgressive inheritance.’; line 178, ‘these genes’ phenotypic traits’; line 193, ‘the gene related to early biomass has pleiotropic effects on all four traits.’; line 215-216, ‘There were no genetic gaps, with adjacent marker separation of no more than 50 cM occurring in each chromosome’; line 329, ‘indicating that QTLs for early biomass on 1DS in this population were new genes located in this study’.

4. Please modify the Figure legends and Table notes to make it easier for readers to understand. For example, line 264, ‘Positive and negative Syn79 and Syn80 alleles produced larger and smaller values, respectively.’

5. It will be good to add the phenotypic data and pictures of AT428 and AT333.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #3: No

PLoS One. 2020 Jun 25;15(6):e0234882. doi: 10.1371/journal.pone.0234882.r004

Author response to Decision Letter 1

23 May 2020

Point-to-point reply to Reviewer #3:

Response: Actually, the mature period of each RIL was mostly similar (often much later than the local cultivars), and the difference between them was slight (Fig. S1-directly photographed from the field at May-11 2020). So, the phenotype evaluation could be collected at one time, as the jointing stage of them were also similar. In this study, Phenotypic data was investigated about 110 days after sowing, when the first internode came out, the plant height and tiller number evaluation were finished during sampling within 1-2 day. Thank you for your careful revision, this should be stated clearly in M & M.

Fig. S1 RILs planted in filed on 2020.

2. About the loci with segregation distortion. Please add the Chi-squared test of the most significant SNPs for each QTL in Table 6.

Response: We performed the Chi-squared test, as was shown in Table 6. For AX-94812958, the Chi-Square value is 38.506 (P<0.001). Chi-Square of AX-109908110 is 57.346 (P<0.001). the Chi-Square value of AX-110910133 is 6.821 (P<0.01). the Chi-Square value of AX-110605376 is 79.258 (P<0.001). the Chi-Square value of AX-109937582 is 82.713 (P<0.001). the Chi-Square of AX-109917900 is 76.722 (P<0.001).

3 and 4. The language also need to be improved, for example, in line 43, change ‘the QTLs’ to ‘these two QTLs’; line 171, ‘There was transgressive inheritance.’; line 178, ‘these genes’ phenotypic traits’; line 193, ‘the gene related to early biomass has pleiotropic effects on all four traits.’; line 215-216, ‘There were no genetic gaps, with adjacent marker separation of no more than 50 cM occurring in each chromosome’; line 329, ‘indicating that QTLs for early biomass on 1DS in this population were new genes located in this study’. 4. Please modify the Figure legends and Table notes to make it easier for readers to understand. For example, line 264, ‘Positive and negative Syn79 and Syn80 alleles produced larger and smaller values, respectively.’

Response: Question 3 and 4 have been fixed in the text.

5. It will be good to add the phenotypic data and pictures of AT428 and AT333.

Response: Unfortunately, we did not introduce the AT428 and AT333 from CIMMYT. However, considering that synthetic hexaploid wheat Syn80 and Syn79 had the same tetraploid parent, their difference of early vigour originated from their diploid parent AT428 and AT333, and the early vigour of AT428 was supposed to be greater than AT333.

Note: The above-mentioned Fig S1 and Table can be found in the attached word file “Response to Reviewers”.

Attachment

Submitted filename: Response to Reviewers.doc

Click here for additional data file.^{(11.7MB, doc)}

PLoS One. doi: 10.1371/journal.pone.0234882.r005

Decision Letter 2

Aimin Zhang

4 Jun 2020

Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

PONE-D-20-04315R2

Dear Dr. Yang,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Aimin Zhang, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #3: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #3: As all comments have been addressed, I suggest that this manuscript can be accepted for publication.

**********

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PLoS One. doi: 10.1371/journal.pone.0234882.r006

Acceptance letter

Aimin Zhang

10 Jun 2020

PONE-D-20-04315R2

Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

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PERMALINK

Mapping QTLs for enhancing early biomass derived from Aegilops tauschii in synthetic hexaploid wheat

Yumin Yang

Hongshen Wan

Fan Yang

Chun Xiao

Jun Li

Meijin Ye

Chunxiu Chen

Guangmin Deng

Qin Wang

Aili Li

Long Mao

Wuyun Yang

Yonghong Zhou

Roles

Abstract

Introduction

Materials and methods https://dx.doi.org/10.17504/protocols.io.bgrnjv5e

Plant materials

Fig 1. Early growth of the two parents and their RILs in the jointing stage.

Field trials

Table 1. Chemical properties of soil in different field trials.

Trait evaluation

SNP genotyping

Statistical and QTL analysis

Results

Phenotypic analysis

Table 2. Parental values, population distribution parameters, and heritability of the investigated traits.

Fig 2. Distribution graph of the phenotypic data for plant height (PH), tiller number per plant (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) under five different environments.

Table 3. Correlation coefficients between the four traits in RILs in different trials.

Genetic map of the D genome

Table 4. SNP markers on the D genome.

Table 5. Segregation distortion of SNP loci in RILs.

QTLs on the D genome

Table 6. QTLs for plant weight (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) in the RILs.

Fig 3. QTLs for plant height (PH), tiller number (TN), shoot fresh weight (SFW) and shoot dry weight (SDW) detected on 1D and 7D in five separate trials.

Discussion

Conclusion

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

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Acceptance letter

Aimin Zhang

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Associated Data

Supplementary Materials

Data Availability Statement

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