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한국 재래종 벼 유묘기 뿌리 발달 전장유전체연관분석

서정환1,2, 장홍지아1, 이아림1, 이원도3, 조유현3, 권순욱1,2, 이주현4,*

Genome-Wide Association Study of Root Development at the Seedling Stage in Korean Landrace Rice

Jeonghwan Seo1,2, Hongjia Zhang1, Ah-Rim Lee1, Wondo Lee3, Yoo-Hyun Cho3, Soon-Wook Kwon1,2, Joohyun Lee4,*
Korean Journal of Breeding Science 2021;53(4):424-431.
Published online: December 1, 2021

1부산대학교 생명자원과학대학 식물생명과학과

2부산대학교 생명산업융합연구원

3농업회사법인 주식회사 시드피아

4건국대학교 식량자원과학과

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*Corresponding Author (E-mail: edmund@konkuk.ac.kr, Tel: +82-2-450-3769, Fax: +82-2-450-3769)
• Received: October 20, 2021   • Revised: October 22, 2021   • Accepted: October 30, 2021

Copyright © 2021 by the Korean Society of Breeding Science

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  • Root development at the seedling stage is an important trait for the early growth of rice. In this study, the root length and weight of 211 Korean landrace rice at the seedling stage were evaluated, and the average root length and weight were 6.94 cm and 48.18 mg, respectively. Principal component analysis (PCA) of 211 accessions based on 70,849 SNPs presented three subgroups. Two quantitative trait loci (QTLs) associated with root length were detected on chromosomes 3 and 6 using genome-wide association study (GWAS). Four haplotypes were identified using associated SNPs for the two root length QTLs. The average root length of Hap2 and Hap 3 was 7.32 cm and 6.56 cm, respectively, and were significantly different. Gene expression analysis in the candidate regions of QTLs for root length at the seedling stage showed that several genes were expressed in the root. QTLs associated with root length at the seedling stage identified in this study may be applied to improve the root length trait and detect candidate genes.
식물의 뿌리는 식물체를 토양에 고정시키고 물과 양분 흡수 및 이동에 중요한 역할을 할 뿐 아니라, 다양한 생물/비생물 스트레스를 감지하고 반응한다(Fukai & Cooper 1995, Gowda et al. 2011). 뿌리 발달은 유전적 요소와 온도, 토양 수분, 토양 염분 및 영양 결핍과 같은 환경 신호에 의해 결정된다(López-Bucio et al. 2003, Yu et al. 2016). 왕성한 뿌리 발달은 양분 흡수를 촉진하여 수량 증대에 기여하므로, 뿌리 발달 개선은 작물 생산성 향상을 위한 중요 목표 형질 중 하나이다(de Dorlodot et al. 2007). 그러므로, 뿌리 발달을 조절하는 유전적 기작에 대한 연구는 고수량 품종의 분자육종을 위해 필요하다. 1995년의 벼 뿌리 형태 QTL 분석 연구(Champoux et al. 1995) 이후 벼 뿌리 발달을 조절하는 유전적 기작이 다양한 방법으로 연구되어 왔다(Jung & McCouch 2013, Mai et al. 2014, Meng et al. 2019).
GWAS 분석은 다양한 유전자원을 활용하여 복잡한 양적형질 조절 유전자를 탐색할 수 있으며, 지난 10여년간 벼에서 양적형질 유전분석 방법 중 하나로 활용되어 왔다(Wang et al. 2020). 벼 뿌리 형질에서도 여러 연구진들이 GWAS 분석 결과를 보고하고 있다. Phung et al. (2016)은 180개 베트남 벼 자원을 이용하여 뿌리 형질들에 대한 GWAS 결과를 보고하였고, Li et al. (2017)은 정상 및 건조 조건에서 다양한 벼 뿌리 발달 관련 형질을 529개 자원과 GWAS 분석을 통해 분석하였다. 본 연구진도 다양한 137개 벼 유전자원으로 구성된 한국 벼 핵심집단(KRICE_CORE, Kim et al. 2016)을 이용하여 유묘기 뿌리 발달 GWAS 분석 결과를 보고한 바 있다(Zhang et al. 2020).
형태적으로 구별되며 역사적 기원을 가지는 재래종은 농민의 다양한 선호도와 지역 환경 적응으로 인해 야생벼에 비해 낮은 유전 다양성을 보이지만 현대 재배종보다는 높은 유전다양성을 나타낸다(Thomson et al. 2007, Pusadee et al. 2009). 이와 더불어 재래종은 풍부한 비생물/생물 저항성과 다른 우수 특성을 가지고 있다. 한국에서는 농촌진흥청 유전자원센터에 약 1,100여점의 재래종 자원이 유지되고 있다. 한국 재래종 벼의 유전 다양성 및 형질 상관에 대한 연구에서, 한국 재래종 벼는 세 개의 하위 그룹으로 구분되며, 14개 형질 중 10개의 형질이 그룹 간에 유의한 차이를 보였다(Li et al. 2014). 하지만 아직까지 국내 재래종으로 구성된 벼 집단을 활용한 농업 형질 GWAS 연구는 미미한 실정이다.
본 연구에서는 국내에서 수집된 재래종 벼 211점을 이용하여 초기 활착 및 생육에 중요한 유묘기 뿌리 발달 관련 GWAS 분석을 수행하였으며, GWAS 분석에서 탐색된 QTL의 haplotype 분석 및 후보 영역의 유전자 발현 분석을 수행하였다.
식물 재료
본 연구에서 유묘기 뿌리 발달 형질 조사 및 전장유전체연관분석을 위해 사용한 국내에서 수집된 재래종 벼 211점의 종자는 농촌진흥청 국립농업과학원 유전자원센터(http://www.genebank.rda.go.kr)에서 분양 받아 사용하였다.
유묘기 뿌리 형질 조사
본 연구에서는 유묘기 뿌리 발달 형질 중 뿌리 길이와 뿌리 무게를 조사하여 전장유전체연관분석에 사용하였다. 각 자원의 종자들은 휴면타파를 위해 3일간 50℃ 처리하였다. 종자 소독 및 발아 촉진을 위해 20분간 차아염소산나트륨(NaClO)에 침지 후 증류수로 3회 세척하였다. 소독된 종자는 페트리 디쉬에 치상하여 30℃에서 3일간 발아시킨 후, 하단부를 자른 96-well PCR 플레이트에 파종하였다. PCR 플레이트는 이틀간 증류수에 띄워 둔 후, Yoshida 양액(Yoshida 1976)으로 옮겼다. 양액의 pH 농도는 염산(HCl)이나 염화나트륨(NaCl)로 5.0-5.5로 조정하였고 매주 새로 갈아주었다. 유묘 생육은 생장 챔버에서 주야간 온도 29℃/21℃와 상대습도 70% 조건에서 이루어졌다. 파종 2주 후 각 재래종 자원에서 5개의 균일한 식물체를 선발하였고, 10일 뒤 5개체의 뿌리 길이와 뿌리 생체중을 측정하였다.
DNA 추출 및 유전자형 분석
한국 재래종 벼 211점의 DNA는 14일된 유묘의 신선한 잎에서 CTAB 방법(Murray & Thompson 1980) 으로 추출하였다. DNA 품질은 아가로즈 젤 전기영동으로 확인하였고, Nanodrop ND-1000 spectrophotometer (Thermo Fisher Scientific, Wilmington, DE, USA)를 사용하여 정량하였다. 한국 재래종 벼 211점에 대한 High-throughput SNP genotyping과 genotype calling은 KNU Axiom Oryza 580K Genotyping Array와 Affymetrix-power-tools를 선행연구에서 기술된 대로 사용하여 수행되었다(Chung et al. 2020). 유전자형 분석 결과는 PLINK (Purcell et al. 2007)를 사용하여 독립적이고 다형성이 있는 SNP만을 필터링 후 분석에는 70,849개의 SNP를 사용하였다.
전장유전체연관분석(Genome-Wide Association Study, GWAS)
한국 재래종 벼 211점의 유전자형 결과를 이용한 주성분분석(Principal Component Analysis, PCA)과 유묘기 뿌리 형질에 대한 GWAS 분석은 GAPIT (Genome Association and Prediction Integrated Tool) (Lipka et al. 2012)을 사용하여 수행하였다. GWAS 분석은 표현형과 유전자형 데이터 및 PCA 결과를 사용하여 일반 선형 모델(General Linear Model, GLM)로 수행하였다. 형질과 SNP의 연관 threshold는 “-log10 (1/number of SNPs)” (Yang et al. 2014) 공식으로 계산하여 -log10(P)=4.85로 설정하였다.
후보 영역 유전자 발현 분석
GWAS 분석에서 탐색된 형질 연관 SNP 부근에서 후보 유전자를 탐색하기 위해 보통 조건에서의 벼 부위별(뿌리, 잎, 생장점, 화기, 종자) RNA 발현 데이터(GEO accession: GSE6893 (Jain et al. 2007))를 NCBI의 GEO database (https://www.ncbi.nlm.nih.gov/geo/)에서 수집하였다. RNA 발현 데이터 중 연관 SNP 좌우 200 kb 후보 영역에서 발현 데이터가 존재하는 유전자들의 부위별 상대적 RNA 발현 양상을 TBtools (Chen et al. 2020)를 이용하여 비교 분석하였다.
유묘기 뿌리 길이 및 무게
한국 재래종 벼 211점의 유묘기 뿌리 발달 변이를 조사하기 위해 파종 24일 후 유묘의 뿌리 길이와 무게를 조사하였다. 뿌리 길이의 평균은 6.94 cm였으며 ‘홍도’의 뿌리 길이가 9.80 cm로 가장 길었고 ‘달골못’의 뿌리 길이가 4.26 cm로 가장 짧았다. 뿌리 무게의 평균은 48.18 mg이고 ‘구안도’의 뿌리 무게가 81.20 mg으로 가장 무거웠으며 ‘아구도’가 19.62 mg로 가장 가벼웠다. 변이계수는 뿌리 길이와 무게에서 각각 16.7%, 27.4%로 나타났다(Table 1). 뿌리 길이와 무게 모두 211점에서 정규분포에 가까운 분포를 보였다(Fig. 1). 이는 한국 재래종 벼의 유묘기 뿌리 길이와 무게에 변이가 존재하며, 관련 유전자 탐색을 위해 양적형질 유전분석이 필요함을 보여준다.
PCA 분석
GWAS 분석에 앞서 한국 재래종 벼 211점의 집단 구조를 확인하기 위해 SNP 70,849개를 사용하여 PCA 분석을 한 결과 211개 한국 재래종 벼는 PC1, 2, 3에 의해 크게 세 가지 하위 그룹으로 나누어 지는 것을 확인하였다(Fig. 2). 이 결과는 394개 한국 재래종 벼를 SSR 마커 29개로 분석하였을 때 3개의 하위 집단으로 구별된 선행연구와 일치하였다(Li et al. 2014). 이는 한국 재래종 벼가 3개의 하위 그룹으로 구별될 수 있음을 나타낸다.
GWAS 분석
GAPIT를 사용하여 유묘기 뿌리 발달 형질 GWAS 분석을 한 결과 유의수준 -Log10(p) ≥ 4.85를 보이는 뿌리 길이와 연관된 두개의 QTL이 염색체 3번과 염색체 6번에서 탐색 되었다. qRL3에서는 33,145,433 bp의 연관 SNP가 -Log10(P) 값 4.89를 보였으며, qRL6에서는 24,247,418 bp의 연관 SNP에서 -Log10(P) 값 5.46을 보였다. 뿌리 길이 관련 두 QTL은 모두 minor allele frequency (MAF) 0.36 이상을 보였고, R2는 모두 0.125 이상이며 두 QTL의 R2 합은 0.265로 나타나, 211개 한국 재래종 벼 뿌리 길이 변이의 약 26.5%를 본 연구에서 탐색된 QTL로 설명할 수 있다. 한편 뿌리 무게와 연관된 유의한 SNP는 탐색되지 않았다(Table 2, Fig. 3). 본 연구진이 핵심집단을 이용하여 유묘기 뿌리 길이와 무게 GWAS 분석을 수행한 선행연구(Zhang et al. 2020)에서 탐색 되었던 QTLs은 본 연구에서 확인되지 않았는데, 이는 GWAS 분석에 사용한 집단의 차이 때문으로 보인다.
본 연구에서 탐색된 뿌리 길이 QTL의 연관 SNP 전후 200 kb 영역을 QTL 후보 영역으로 간주했을 때, QTL 후보 영역에서 기존 보고된 뿌리 길이와 직접적으로 연관된 QTL이나 유전자는 없었다. 하지만 외부 스트레스 및 토양 환경에 의해 뿌리 발달이 조절 되기에 이와 관련된 보고가 있는 유전자들을 후보 유전자로 정리하였다. qRL3 연관 SNP의 171~157 kb 위 쪽에 세 개의 스트레스 연관 단백질(stress associated protein, SAP) 유전자(OsSAP6, OsSAP7, OsSAP7)가 함께 존재하였고(Muthuramalingam et al. 2021), 121 kb 아래 쪽에서 염 스트레스 조건에서 강하게 유도되며 과발현 식물체의 염해 내성이 증가된 OsSIRP2 유전자가 보고 되었다(Chapagain et al. 2018). qRL3 연관 SNP 145 kb 위 쪽에서는 casein kinase-I (CK1) 단백질을 암호화 하며, 출수기를 조절하는 Hd16/EF1 유전자가 위치했는데(Dai & Xue 2010, Hori et al. 2013), 최근 이 유전자의 nonfunctional allele이 보통 조건에서 뿐 아니라 저양분 조건에서도 생육을 촉진시킨다는 보고가 있었다(Tanaka et al. 2019).
qRL6 영역 연관 SNP 65 kb 아래쪽의 SNP S6_24313195는 분얼을 조절하는 MOC1 유전자의 인트론에 위치하였으며(Li et al. 2003), 최근 액생분열조직의 MOC1 단백질이 식물 호르몬을 통한 길항적 뿌리 및 분얼 생육의 매개체 중 하나로 역할 한다는 것이 보고되었다(Lin et al. 2020). 본 연구에서 확인한 QTL 영역의 후보 유전자들은 추후 분리집단 또는 형질전환체를 이용한 검증 후 뿌리 형질 개선에 적용될 수 있을 것이다.
Haplotype 분석
본 연구에서 탐색된 뿌리 길이 QTL 두 개의 조합 효과를 확인하기 위해 연관 SNP 두 개를 이용하여 haplotype 분석을 실시한 결과 총 네 개의 haplotype으로 구별되었다. 이 중 Hap2가 평균 7.32 cm로 뿌리 길이가 가장 길었고, Hap3가 평균 6.56 cm로 뿌리 길이가 가장 짧았으며, 두 haplotype 간에서만 유의한 차이가 있었다(Table 3). 뿌리 길이 8.50 cm 이상인 15개 자원에서 Hap1 3개, Hap2 7개, Hap3 2개, Hap4 3개가 분포하여 Hap2를 가진 자원들의 뿌리 길이가 긴 경향을 보였다(Table 4). Haplotype 결과에 따라 추후 유묘기 뿌리 길이 개선에 Hap2를 가진 자원들을 활용할 수 있을 것이다.
후보 영역 유전자 발현 분석
GWAS 분석에서 탐색된 뿌리 길이 관련 QTL 영역에서 후보 유전자를 탐색하기 위해 연관 SNP 전후 200 kb 후보 영역의 유전자 발현 분석을 공개된 RNA 발현 데이터를 활용하여 수행하였다. 6번 염색체에서는 후보 영역에 37개의 유전자에 대한 발현 데이터가 있었으며, 3번 염색체에서는 51개 유전자의 발현 데이터가 후보 영역에 있었다. 유전자들의 상대적인 발현을 뿌리, 성숙한 잎, 어린 잎, 지상부, 생장점, 어린 이삭, 성숙한 이삭, 종자의 7개 부위별로 비교 하였다(Fig. 4). 두 염색체의 후보 영역에서 모두 뿌리에서 강력하게 발현하는 유전자들을 확인할 수 있었으며, 일부 유전자는 뿌리에서만 발현되는 것을 확인하였다. 특히 qRL3 영역에 위치한 스트레스 연관 유전자 OsSAP7 유전자(Os03g0793000)과 출수 및 양분 흡수 관련 Hd16/EF1 유전자(Os03g0793500)는 뿌리에서 가장 많이 발현하여 추후 유묘기 뿌리 발달 유전자 검증의 강력한 후보유전자로 보인다(Fig. 4). 반면, qRL6 영역의 MOC1 유전자의 발현 데이터는 확인할 수 없었다. 향후 본 연구에서 확인한 후보 영역의 정보를 활용하여 뿌리 길이 조절 후보 유전자 검증 및 뿌리 발달 기능 연구에 활용하고자 한다.
한국 재래종 벼 211점에 대한 유묘기 뿌리 길이와 무게를 조사한 결과, 뿌리 길이의 평균은 6.94 cm였고 뿌리 무게의 평균은 48.18 mg이었다. SNP 70,849개를 사용하여 PCA 분석을 한 결과 한국 재래종 벼 211점은 세 개의 하위 그룹으로 구별되었다. GWAS 분석에서 뿌리 길이 연관 QTL 두 개가 3번과 6번 염색체에서 탐색 되었다. 뿌리 길이 QTL의 연관 SNP 두 개를 이용한 Haplotype 분석 결과 네 개의 haplotype이 확인 되었고, 이중 Hap2와 Hap3의 평균 뿌리 길이가 각각 7.32 cm와 6.56 cm로 서로 유의한 차이가 있었다. 뿌리 길이 QTL 후보 영역의 유전자 발현 분석에서 뿌리에서 발현하는 유전자들을 확인할 수 있었다. 본 연구에서 탐색된 벼 유묘기 뿌리 길이 연관 QTL 정보는 향후 벼 유묘기 뿌리 길이 형질 개선 및 후보 유전자 탐색에 활용될 것이다.
본 연구는 농촌진흥청 차세대농작물신육종기술개발사업_신육종 기반기술 개발사업(PJ01480502)의 지원으로 수행되었습니다.
Fig. 1
Histogram for root length (A) and root weight (B) of 211 Korean landrace rice.
KJBS-53-424-f1.tif
Fig. 2
3D scatter plot for principal components of the 211 Korean landrace rice.
KJBS-53-424-f2.tif
Fig. 3
Manhattan plot for root length (A) and root weight (B) of 211 Korean landrace rice using GAPIT. The threshold of significant -log10(P) is 4.85 and red arrows indicate significantly associated SNPs.
KJBS-53-424-f3.tif
Fig. 4
Gene expression in different rice tissues using RNA expression data. Red and blue color represent the high and low expression, respectively. (A) Genes on chromosome 3. (B) Genes on chromosome 6.
KJBS-53-424-f4.tif
Table 1
Basic statistics of root length (RL) and root weight (RW) at seeding stage in 211 Korean landrace rice.
Table 1
RL (cm) RW (mg)
Maximum 9.80 (Hongdo) 81.20 (Guando)
Minimum 4.26 (Dalgolmot) 19.62 (Agudo)
Average±SD 6.94±1.16 48.18±13.2
Coefficient of variation (%) 16.7 27.4
Table 2
List of association sites for root length (RL) identified in current study.
Table 2
Trait QTL Associated SNP Chr Position -Log10(P) MAFz R2 Reported gene
RL qRL3 S3_33145433 3 33,145,433 4.89 0.450 0.125 OsSAP6, OsSAP7, OsSAP14, Hd16/EF1, OsSIRP2
RL qRL6 S6_24247418 6 24,247,418 5.46 0.366 0.140 MOC1

zMinor allele frequency

Table 3
Haplotype analysis for root length using associated two SNPs identified in this study. The significance test was conducted using Tukey’s test.
Table 3
SNP ID S3_33145433 S6_24247418 Number of accessions Average root length
Chromosome 3 6
Position 33,145,433 24,247,418
Allele C/T C/T
Hap1 C C 54 6.81±1.18ab
Hap2 T C 67 7.32±1.01a
Hap3 C T 51 6.56±1.15b
Hap4 T T 19 7.05±1.33ab
Table 4
15 accessions showing more than 8.50 cm for root length at seedling stage among 211 Korean landrace rice.
Table 4
Haplotype IT Number Name Root length (cm)
Hap1 009118 Hongdo 9.80
008267 Jangsamdo 9.78
006818 Susangjo 8.79
Hap2 010374 Sando 9.68
010582 Jaeraeyukdo 9.70
008530 Joseondo 8.77
008804 Cheonjeungdo 8.72
006522 Buljo 8.78
008579 Jojeongdo 8.60
009142 Hwado 9.60
Hap3 009120 Hongdodo 8.50
007254 Sujungjo 9.73
Hap4 006005 Ddangbyeo 9.35
005689 Dadeogbereumbyeo 9.52
007592 Yeosubyeo 9.38
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Genome-Wide Association Study of Root Development at the Seedling Stage in Korean Landrace Rice
Korean. J. Breed. Sci.. 2021;53(4):424-431.   Published online December 1, 2021
DOI: https://doi.org/10.9787/KJBS.2021.53.4.424
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Korean. J. Breed. Sci.. 2021;53(4):424-431.   Published online December 1, 2021
DOI: https://doi.org/10.9787/KJBS.2021.53.4.424
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Genome-Wide Association Study of Root Development at the Seedling Stage in Korean Landrace Rice
Image Image Image Image
Fig. 1 Histogram for root length (A) and root weight (B) of 211 Korean landrace rice.
Fig. 2 3D scatter plot for principal components of the 211 Korean landrace rice.
Fig. 3 Manhattan plot for root length (A) and root weight (B) of 211 Korean landrace rice using GAPIT. The threshold of significant -log10(P) is 4.85 and red arrows indicate significantly associated SNPs.
Fig. 4 Gene expression in different rice tissues using RNA expression data. Red and blue color represent the high and low expression, respectively. (A) Genes on chromosome 3. (B) Genes on chromosome 6.

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Genome-Wide Association Study of Root Development at the Seedling Stage in Korean Landrace Rice

Basic statistics of root length (RL) and root weight (RW) at seeding stage in 211 Korean landrace rice.

RL (cm) RW (mg)
Maximum 9.80 (Hongdo) 81.20 (Guando)
Minimum 4.26 (Dalgolmot) 19.62 (Agudo)
Average±SD 6.94±1.16 48.18±13.2
Coefficient of variation (%) 16.7 27.4

List of association sites for root length (RL) identified in current study.

Trait QTL Associated SNP Chr Position -Log10(P) MAFz R2 Reported gene
RL qRL3 S3_33145433 3 33,145,433 4.89 0.450 0.125 OsSAP6, OsSAP7, OsSAP14, Hd16/EF1, OsSIRP2
RL qRL6 S6_24247418 6 24,247,418 5.46 0.366 0.140 MOC1

Haplotype analysis for root length using associated two SNPs identified in this study. The significance test was conducted using Tukey’s test.

SNP ID S3_33145433 S6_24247418 Number of accessions Average root length
Chromosome 3 6
Position 33,145,433 24,247,418
Allele C/T C/T
Hap1 C C 54 6.81±1.18ab
Hap2 T C 67 7.32±1.01a
Hap3 C T 51 6.56±1.15b
Hap4 T T 19 7.05±1.33ab

15 accessions showing more than 8.50 cm for root length at seedling stage among 211 Korean landrace rice.

Haplotype IT Number Name Root length (cm)
Hap1 009118 Hongdo 9.80
008267 Jangsamdo 9.78
006818 Susangjo 8.79
Hap2 010374 Sando 9.68
010582 Jaeraeyukdo 9.70
008530 Joseondo 8.77
008804 Cheonjeungdo 8.72
006522 Buljo 8.78
008579 Jojeongdo 8.60
009142 Hwado 9.60
Hap3 009120 Hongdodo 8.50
007254 Sujungjo 9.73
Hap4 006005 Ddangbyeo 9.35
005689 Dadeogbereumbyeo 9.52
007592 Yeosubyeo 9.38
Table 1 Basic statistics of root length (RL) and root weight (RW) at seeding stage in 211 Korean landrace rice.
Table 2 List of association sites for root length (RL) identified in current study.

zMinor allele frequency

Table 3 Haplotype analysis for root length using associated two SNPs identified in this study. The significance test was conducted using Tukey’s test.
Table 4 15 accessions showing more than 8.50 cm for root length at seedling stage among 211 Korean landrace rice.

Table 1

Table 2

Table 3

Table 4

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