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벼 담수발아 내성 관련 양적형질 유전자좌 탐색

장성규1,2, 김용철1, 권순욱1,2,*

Detection of QTLs related to submergence tolerance on germination stage in rice (Oryza sativa L.)

Seong-Gyu Jang1,2, Yongchul Kim1, Soon-Wook Kwon1,2,*
Korean Journal of Breeding Science 2022;54(4):369-374.
Published online: December 1, 2022

1부산대학교 식물생명과학과

2부산대학교 생명산업융합연구원

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*Corresponding Author: (E-mail: swkwon@pusan.ac.kr, Tel: +82-55-350-5506, Fax: +82-55-350-5509)
• Received: November 8, 2022   • Revised: November 14, 2022   • Accepted: November 14, 2022

Copyright © 2022 by the Korean Society of Breeding Science

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  • Submergence is becoming a major problem in decreasing rice production. This study conducted a QTL analysis for submergence tolerance on germination stage using 165 recombinant inbred lines (RILs) derived from crosses between ‘Milyang 23’ and ‘Tong 88-7’. An integrated genetic linkage map consisting of 1,313 SNPs was constructed, which covered a total length of 1,254.59 cM, with an average distance of 0.96 cM between adjacent markers. Four QTLs were detected on chromosomes 1, 3, 4, and 7. In qSUB1 and qSUB3, the allele of ‘Tong88-7’ improved survival rates, while in qSUB4 and qSUB7 the allele of ‘Milyang 23’ improved the same. Phenotypic variance explanations for qSUB1, qSUB3, qSUB4, and qSUB7 were 9.44%, 14.62%, 9.74%, and 7.09%, respectively. The average survival rate of the lines with all four QTLs was 93.33±6.67%.
벼는 전 세계적으로 많이 이용하고 있는 주요 식량공급원 중 하나로 전 세계 인구 절반이 주식으로 사용하고 있다(Pandey et al. 2002, Samal et al. 2018). 하지만 강우량이 많은 저지대 대부분 지역과 남아시아와 동남아시아의 일부 관개지역은 범람에 취약하여 막대한 손실이 발생되고 있는 것으로 보고되고 있으며, 기후변화로 인해 더 악화될 수 있을 것으로 예상되고 있다(Singh et al. 2011, Redfern et al. 2012). 특히, 낮은 비용과 편리성 때문에 많은 국가에서 직파재배를 이용하고 있으나, 침수취약지역에서는 파종 후 침수피해가 발생하는 경우가 흔하며, 담수발아 내성을 지닌 품종을 육종하는 것이 도움이 될 것으로 보고되고 있다(Yamauchi et al. 1993, Angaji et al. 2010).
일반적으로 벼는 침수가 5일 이상 지속이 되면 고사되기 시작하는 것으로 보고되고 있으며, 침수된 상태의 토양에서 발아하는 종자는 저산소 스트레스로 인해 효소가 기능하지 않게 되어 종자의 발아와 후속 생육에 방해를 받게 된다(Mackill et al. 2010, Mondal et al. 2020). 담수 조건으로 인한 산소와 이산화탄소의 공급 차단은 벼의 호흡과 광합성을 제한한다. 침수저항성 자원의 경우, 절간신장을 유도하거나 잎 면적을 줄여 초엽의 성장을 촉진시키고 수면에 도달하도록 함으로써 뿌리의 산소결핍 피해를 최소화시키는 것으로 보고되고 있다(Panda et al. 2008, Yamauchi et al. 2018).
침수로 인한 피해를 최소화하기 위해 국제미작연구소(International Rice Research Institute: IRRI)에서는 침수저항성 유전자 ‘Sub1’을 도입한 품종(Swarna-Sub1, IR64-Sub1, Samba Mahsuri-Sub1, BR11-Sub1, TDK1-Sub1 및 CR1009-Sub1)을 개발하였으나(Septiningsih et al. 2015, Iftekharuddaula et al. 2016), 기작이 매우 복잡한 것으로 보고되고 있다. 또한 저항성을 가진 유전자원이 많지 않고, 주동유전자의 발견이 어려운 것으로 보고되고 있으며, 인디카 또는 잡초벼에서 유래하는 경우가 많다고 한다(Redoña & Mackill 1996, Yamauchi & Winn 1996, Biswas & Yamauchi 1997, Kim et al. 2019).
Angaji et al. (2010)은 벼 발아기때 침수피해를 줄이기 위해 담수발아 내성을 지닌 미얀마 잡초벼 ‘Khao Hlan On’에 ‘IR64’를 반복친으로 교배하여 423개의 BC2F2 집단을 육성하였으며, 135개의 SSR마커를 사용하여 해당 집단에 대한 유전자지도를 완성하였다. QTL분석을 통해 총 4개의 염색체 상에서 5개의 QTL을 탐색하였으며, 각각 qAG-1-2, qAG-3-1, qAG-7-2, qAG-9-1 및 qAG-9-2를 보고하였다. Singh et al. (2017)은 침수저항성을 지닌 ‘Ciherang-Sub1’과 ‘IR10F365’을 교배하여 148개의 RIL집단을 구축하였으며, 침수상태에서 15개의 농업형질을 조사하여 침수상태에서 유리한 형질의 주요 QTL부위를 3번 염색체 상과 5번 염색체 상에서 탐색하였다. 다른 연구팀에서는 인도 재래품종인 ‘Rashpanjor’에서 침수 조건에서 높은 생존율을 확인하였고, 고수량성 품종인 ‘Swarna’와 교배하여 180개 RIL집단을 육성하였다. QTL분석을 통해 17개 QTL을 탐색하였고, 이들은 전체 표현형 변이의 6.53~57.89% 를 설명하였다. 해당 QTL 영역에서 탐색된 후보유전자에서 에틸렌 생합성과 Auxin등의 대사물질과 연관된 부위가 많은 것으로 보고하였다(Chattopadhyay et al. 2021).
본 연구는 담수발아 관련 QTL을 탐색하기 위하여 ‘밀양23호’, ‘Tong88-7’, 165개 RIL집단에 대해 담수발아시 생존율을 평가하고, 총 1,313개 SNP를 이용하여 담수발아 내성 관련 QTL 탐색 및 각각 QTL의 효과를 규명하기 위해 수행되었다.
식물 재료
본 연구에서 담수발아 내성 QTL 분석을 위하여 ‘밀양 23호’와 ‘Tong88-7’의 인공교배를 통해 육성된 165개 재조합 집단(Recombinant Inbred Line; RIL)을 공시하였다(Jiang et al. 2011). ‘Tong88-7’은 중국 남부지역에서 유래된 온대 자포니카 품종으로 침수저항성을 지니고 있는 것을 확인하였고, ‘밀양 23호’는 통일벼 품종으로 침수 조건에 대해 감수성을 보였다. 두 모본과 165개 RIL은 2021년에 부산대학교 부속농장 시험포장에서(경상남도 밀양) 표준재배법으로 증식한 후, 본 연구의 재료로 사용하였다. 수확된 종자는 통풍이 잘 되는 온실에서 건조 후, 저온 저장고에 보관하였으며 매 실험마다 발아적온(30℃)에서 발아 검정을 통하여 정상 발아 정도를 평가한 후 침수 처리를 하였다.
담수발아 내성 특성 평가
‘밀양 23호’와 ‘Tong88-7’ 및 165개 RIL 집단의 담수발아 내성 검정은 Kim et al. (2019)와 Angaji et al. (2010)의 방법을 참고하여 담수발아시 생존율을 평가하였다. 수도용 플라스틱 파종 상자(50공)에 수도용 상토를 채운 후 계통 당 30개의 마른 종자를 3개의 파종 구멍에 각 10개씩 나누어 파종한 후 1 cm 두께로 복토하였다. 이후 담수를 위하여 파종 상자를 저수용 상자(길이×너비×깊이; 67×50.5×41.5 cm)로 옮긴 후 수심 10 cm 깊이로 담수 처리 후 시험기간 동안 수심을 유지하였다. 침수처리는 평균온도가 21℃로 설정된 온실에서 수행하였으며, 파종 21일 후 수면위로 초엽이 출현한 개체를 생존 개체로 판단하여 생존율을 계산하였다.
DNA 추출 및 유전자형 분석
DNA 추출은 이앙 전 유묘의 잎을 채취하여 CTAB (cetyltrimethyl ammonium bromide) 방법으로 추출하였다(Murray & Thompson 1980). 잎 2 g을 막자사발에 놓고 액체 질소에 침적시킨 후 마쇄하였다. 600 μL의 CTAB solution을 넣고, 65℃ Dry bath (DAIHAN Scientific, South Korea)에 10분간 넣어 두었다. 500 μL CI 용액(chloroform : isoamyl alcohol=24 : 1)을 첨가 후 12,000 rpm으로 3분간 원심분리하여 400 μL 상등액을 1.5 mL tube에 옮겼다. 400 μL의 isopropyl alcohol을 첨가하여 2~3회 혼합한 후, -20℃에 3시간 반응 후 12,000 rpm에서 3분간 원심분리 하였다. 상등액을 버리고 700 μL 70% ethyl alcohol로 2회 세정 후 건조하였으며, TE buffer (10 mM Tris-HCL, pH 8.0, 2.5 mM EDTA)에 녹인 후 유전자형 분석에 이용했다. RIL 집단의 유전자형 분석은 Illumina Infinium rice 6K SNP chip 칩을 이용하여 분석하였다(Thomson 2014).
연관지도(Linkage map) 작성과 QTL 분석
연관지도는 ‘밀양 23호’와 ‘Tong88-7’에서 다형성을 나타내는 1,313개 SNP에 대해 IciMapping ver. 4.1 (Chinese Academy of agricultural Sciences, China)를 이용하여 작성하였다(Meng et al. 2015). CIM (Composite interval mapping) 방법으로 QTL분석을 수행하였고, 유의한 QTL의 존재를 결정하기 위한 LOD의 임계값은 p≤0.05 조건에 1000반복으로 permutation test에 의해 결정하였다(Churchill & Doerge 1994). 후보 유전자 검색은 Rap-db (http://rapdb.dna.affrc.go.jp)을 이용하였다. 형질의 평균 등 기술통계, t-test, Duncan's Multiple Range Test의 통계분석은 R (Version 4.2.1, The R Foundation for Statistical Computing Platform)을 이용하였다.
담수발아 내성 검정과 유전자 지도 작성
담수발아 내성과 관련된 QTL부위를 탐색하기위해 두 모본과 165개 RIL에 저항성 검정을 실시하였다. 수심 10 cm의 침수조건에서 ‘밀양23호’와 ‘Tong88-7’의 생존율이 각각 6.67%와 73.33%로 자포니카 품종인 ‘Tong-88-7’이 통일형 품종인 ‘밀양 23호’보다 높은 생존율을 보였다. 165개의 RIL 집단의 생존율 분포는 0~ 100%로 나타났으며 평균 생존율은 50.28%로 나타났다(Fig. 1).
‘밀양23호’와 ‘Tong88-7’에서 다형성을 보이는 총 1,313의 SNP를 선발하였고, 해당 SNP 정보를 이용하여 RIL집단의 연관지도를 작성하였다. 전체 염색체 길이는 1254.59 cM으로 마커간 평균 거리는 0.96 cM이었다(Fig. 2).
QTL 분석
담수발아 내성과 관련된 QTL 탐색을 위하여 permutation test의 LOD값 3.1이상인 QTL을 선발하였다. 염색체 1번, 3번, 4번, 7번에서 각각 한 개씩 총 4개의 QTL (qSUB1, qSUB3, qSUB4, qSUB7)이 탐색되었으며, 전체 표현형 변이의 설명력은 7.09~14.61%이었고, qSUB3 > qSUB4 > qSUB1 > qSUB7 순으로 표현형 변이에 대한 설명력이 높았다. qSUB1은 01_id0021와 01_id0022 사이에 위치하였고, ‘Tong88-7’ 대립유전자형에 의해 담수발아 내성이 향상되었다. LOD는 5.07이고, 8.40% 생존율을 증가시키는 효과를 보였다. qSUB3은 03_id0470와 03_id0471 사이에 위치하며, 전체 표현형 변이가 제일 높은 14.62%를 설명하였고, ‘Tong88-7’ 대립유전자형에 의해 10.67%의 생존율을 증가시키는 효과가 있었다. 4번 염색체 04_id0604와 04_id0605에서 탐색된 qSUB4는 ‘밀양23호’ 대립유전자형이 담수발아 내성을 향상시키는 것으로 나타났으며, 5.22의 LOD값과 8.57% 생존율 증가를 보였다. qSUB7은 07_id0855와 07_id0856에서 탐색된 QTL로 3.69의 LOD값과 7.27%의 생존율 증가를 보였으며, ‘밀양23호’ 대립유전자형이 담수발아 내성을 향상시키는 것으로 나타났다(Table 1, Fig. 2). 특히, qSUB3 영역에는 OsERS1 유전자가 존재하며 생리적 활동을 조절하는 호르몬인 에틸렌이 관련되어 있고, 벼가 침수 시 뿌리 성장을 억제하고 잎의 신장을 촉진시키는 것으로 보고되었다(Pareek et al. 2006, Yu et al. 2017). Yin et al. (2017)은 에틸렌이 벼가 침수에 적응하도록 돕는 대사물질로서 증가된 에틸렌은 SK1 (snorkel1)과 SK2 (snorkel2) 의 발현을 상향 조절하여 침수조건에서 벼의 절간신장을 촉진시킨다고 보고했다.
QTL 조합에 따른 파종 후 담수발아 내성 효과 분석
탐색된 담수발아 내성 관련 4개의 QTL, qSUB1, qSUB3, qSUB4, qSUB7의 QTL별 생존율과 이들 QTL의 집적 효과를 조합별로 분석하였다. QTL영역에서 LOD 값이 가장 높은 곳에 위치한 분자 마커들을 각각 선발하였고, 이들을 이용한 QTL의 집적 여부에 따라 밀양23호/Tong88-7 RIL집단을 총 15개의 그룹으로 나누었다(Table 2). 어떠한 QTL도 집적되지 않은 그룹1은 20.00±17.52% 생존율을 보였고 같은 수준의 생존율을 보였던 그룹2, 4, 5의 qSUB1, qSUB4, qSUB7은 56.66±24.11%, 63.07±20.77, 58.69±24.38로 그룹1보다 높은 생존율을 보였다. 그룹3의 qSUB3 (63.07±20.77)은 2종류의 QTL이 집적된 수준과 같은 수준의 생존율을 보였으며, 3종류의 QTL이 집적된 생존율은 그룹13 (73.33±13.39), 그룹14 (78.33±14.43), 그룹12 (80.83± 19.56) 순으로 강하게 나타났다. 최종적으로 모든 QTL집적된 그룹15는 93.33±6.67%로 가장 높은 수준의 생존율을 보여 담수발아 내성이 가장 높게 향상된 것으로 조사되었다(Table 2, Fig. 3). 따라서 본 연구에서 탐색된 QTL의 집적을 통해 담수 발아시 침수에 따른 입모율 감소를 경감시킬 수 있을 것으로 기대된다. 특히 ‘밀양23호’ 유래된 qSUB4, qSUB7은 국내 자포니카 품종의 직파재배시 초기 입모율 향상을 위한 유용한 육종 재료가 될 것으로 기대된다.
본 연구는 밀양23호/Tong88-7 RIL집단을 이용하여 담수 발아조건에서의 생존율에 대해 QTL분석을 수행하였다. 유전자 연관지도는 두 모본에서 다형성을 보인 1,313개 SNP로 작성되었고, 전체 염색체 크기는 1254.59 cM으로 마커간 평균 거리는 0.96 cM이었다. 담수발아 내성과 관련된 4개의 QTL이 탐색되었고, qSUB1과 qSUB3이 ‘Tong88-7’의 대립유전자형이 담수발아 내성을 향상시켰고, qSUB4과 qSUB7은 ‘밀양23호’ 대립유전자가 담수발아 내성을 향상시키는 것으로 나타났다. qSUB1, qSUB3, qSUB4, qSUB7의 전체 표현형 변이에 대한 설명력은 각각 9.44%, 14.62%, 9.74%, 7.09%로 나타났다. 4개의 QTL이 모두 집적된 계통의 평균 생존율이 93.33±6.67%로 가장 높았다.
본 연구는 농촌진흥청 작물분자육종 생명공학 혁신기술 개발사업(PJ01579403)의 지원으로 수행되었습니다.
Fig. 1
Submergence tolerance phenotype of ‘Milyang23’, ‘Tong88-7’ and RILs at germination stage.
kjbs-54-4-369-f1.jpg
Fig. 2
Linkage maps composed of 1313 SNP markers for flooding tolerance in 165 RIL population. Three flooding tolerance QTLs were detected on chromosomes 1, 3, 4, and 7 from the milyang23/Tong88-7 RIL population after seeding emergence. The linkage map was generated using QTL IciMapping program ver. 4.1.
kjbs-54-4-369-f2.jpg
Fig. 3
The survival rate of the Milyang23/Tong88-7 RILs carrying different allele combinations of qSUB1, qSUB3, qSUB4, and qSUB7. Letters from a to d indicate significantly different values according to duncan's multiple range test (α=0.05). Errors bars indicate the standard errors of each category.
kjbs-54-4-369-f3.jpg
Table 1
QTLs of seedling flooding tolerance in RIL population derived from a cross milyang23 and Tong88-7 depends after seeding emergence.
Table 1
QTLs Chromosome Position (cM) LeftMarker RightMarker LODz PVEy(%) Addx
qSUB1 1 11.85-12.19 01_id0021 01_id0022 5.07 9.44 8.40
qSUB3 3 83.57-84.59 03_id0470 03_id0471 7.53 14.62 10.67
qSUB4 4 107.91-108.23 04_id0604 04_id0605 5.22 9.74 -8.57
qSUB7 7 54.48-55.51 07_id0855 07_id0856 3.69 7.09 -7.27

zLOD: The logarithm of the odds

yPVE: Percentage of the phenotypic variance that was explained.

xAdd: Positive value of the additive effect indicate that allele from ‘Tong88-7’ was in the direction of increasing the trait value.

Table 2
QTL pyramiding effect on flooding tolerance after seeding emergence. Letters from a to d indicate significantly different values according to duncan's multiple range test (α=0.05).
Table 2
Group QTL No. of lines Survival rate
(Mean±SD)
1 Non 11 20.00±17.52d
2 qSUB1 58 56.66±24.11c
3 qSUB3 52 63.07±20.77bc
4 qSUB4 79 57.95±24.38c
5 qSUB7 61 58.69±24.38c
6 qSUB1+qSUB3 18 71.85±17.15bc
7 qSUB1+qSUB4 31 65.38±21.84bc
8 qSUB1+qSUB7 21 60.00±22.70bc
9 qSUB3+qSUB4 27 69.38±20.87bc
10 qSUB3+qSUB7 27 69.38±20.86bc
11 qSUB4+qSUB7 35 67.62±21.68bc
12 qSUB1+qSUB3+qSUB4 8 80.83±19.56ab
13 qSUB1+qSUB3+qSUB7 5 73.33±13.39bc
14 qSUB3+qSUB4+qSUB7 12 78.33±14.43abc
15 qSUB1+qSUB3+qSUB4+qSUB7 2 93.33±6.67a
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Detection of QTLs related to submergence tolerance on germination stage in rice (Oryza sativa L.)
Korean. J. Breed. Sci.. 2022;54(4):369-374.   Published online December 1, 2022
DOI: https://doi.org/10.9787/KJBS.2022.54.4.369
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Detection of QTLs related to submergence tolerance on germination stage in rice (Oryza sativa L.)
Korean. J. Breed. Sci.. 2022;54(4):369-374.   Published online December 1, 2022
DOI: https://doi.org/10.9787/KJBS.2022.54.4.369
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Detection of QTLs related to submergence tolerance on germination stage in rice (Oryza sativa L.)
Image Image Image
Fig. 1 Submergence tolerance phenotype of ‘Milyang23’, ‘Tong88-7’ and RILs at germination stage.
Fig. 2 Linkage maps composed of 1313 SNP markers for flooding tolerance in 165 RIL population. Three flooding tolerance QTLs were detected on chromosomes 1, 3, 4, and 7 from the milyang23/Tong88-7 RIL population after seeding emergence. The linkage map was generated using QTL IciMapping program ver. 4.1.
Fig. 3 The survival rate of the Milyang23/Tong88-7 RILs carrying different allele combinations of qSUB1, qSUB3, qSUB4, and qSUB7. Letters from a to d indicate significantly different values according to duncan's multiple range test (α=0.05). Errors bars indicate the standard errors of each category.

Fig. 1

Fig. 2

Fig. 3

Detection of QTLs related to submergence tolerance on germination stage in rice (Oryza sativa L.)

QTLs of seedling flooding tolerance in RIL population derived from a cross milyang23 and Tong88-7 depends after seeding emergence.

QTLs Chromosome Position (cM) LeftMarker RightMarker LODz PVEy(%) Addx
qSUB1 1 11.85-12.19 01_id0021 01_id0022 5.07 9.44 8.40
qSUB3 3 83.57-84.59 03_id0470 03_id0471 7.53 14.62 10.67
qSUB4 4 107.91-108.23 04_id0604 04_id0605 5.22 9.74 -8.57
qSUB7 7 54.48-55.51 07_id0855 07_id0856 3.69 7.09 -7.27

QTL pyramiding effect on flooding tolerance after seeding emergence. Letters from a to d indicate significantly different values according to duncan's multiple range test (α=0.05).

Group QTL No. of lines Survival rate
(Mean±SD)
1 Non 11 20.00±17.52d
2 qSUB1 58 56.66±24.11c
3 qSUB3 52 63.07±20.77bc
4 qSUB4 79 57.95±24.38c
5 qSUB7 61 58.69±24.38c
6 qSUB1+qSUB3 18 71.85±17.15bc
7 qSUB1+qSUB4 31 65.38±21.84bc
8 qSUB1+qSUB7 21 60.00±22.70bc
9 qSUB3+qSUB4 27 69.38±20.87bc
10 qSUB3+qSUB7 27 69.38±20.86bc
11 qSUB4+qSUB7 35 67.62±21.68bc
12 qSUB1+qSUB3+qSUB4 8 80.83±19.56ab
13 qSUB1+qSUB3+qSUB7 5 73.33±13.39bc
14 qSUB3+qSUB4+qSUB7 12 78.33±14.43abc
15 qSUB1+qSUB3+qSUB4+qSUB7 2 93.33±6.67a
Table 1 QTLs of seedling flooding tolerance in RIL population derived from a cross milyang23 and Tong88-7 depends after seeding emergence.

zLOD: The logarithm of the odds

yPVE: Percentage of the phenotypic variance that was explained.

xAdd: Positive value of the additive effect indicate that allele from ‘Tong88-7’ was in the direction of increasing the trait value.

Table 2 QTL pyramiding effect on flooding tolerance after seeding emergence. Letters from a to d indicate significantly different values according to duncan's multiple range test (α=0.05).

Table 1

Table 2

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