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Powdery mildew (Blumeria graminis f. sp. tritici) significantly affects wheat yield and flour quality. Plant resistance to powdery mildew has been investigated for decades, and numerous resistance genes and quantitative trait loci (QTLs) for molecular markers have been discovered. In Korea, powdery mildew occurs initially in spring, due to frequent rain and low temperatures, becoming severe during the harvest season. In Korea, systematic monitoring and quantitative and qualitative impact assessments of powdery mildew outbreaks have never been conducted properly. Herein, the lifecycle of powdery mildew, resistance genes, QTLs, and selection markers in wheat were examined to elucidate powdery mildew resistance, develop resistant varieties, and genetic markers suitable for the domestic environment.
현재까지 밀에서는 63개의 유전자좌에서 100개이상의 Pm유전자/대립유전자와 100개 이상의 양적유전자좌(quantitative trait loci, QTL)가 보고되었으며 이를 통한 흰가루병 저항성 유용자원 탐색 및 저항성 품종 육성과 육종 효율성 증진에 많은 노력을 기울이고 있다(Asad et al. 2014, Gao et al. 2018, Kang et al. 2020, McIntosh et al. 2017Mwale et al. 2014, Shah et al. 2018, Tang et al. 2018). 우리나라의 흰가루병 발생은 강수량과 포장의 과습 상태에 따른 발생이 연차간 지역간 차이가 클 것으로 예측되지만, 체계적인 예찰이나 흰가루병 발생에 따른 수량 및 품질에 미치는 영향에 대한 평가는 제대로 이루어진 적이 없는 실정이다. 국내에서도 기후변화와 밀산업육성법 제정으로 어느때 보다 안정적인 국산밀 생산이 중요하기 때문에, 본 연구에서는 흰가루병 저항성 증진에 관련된 최근 연구 동향을 정리하여 흰가루병에 대한 이해와 저항성 유용자원 탐색 및 품종육성에 도움이 되고자 하였다.
본 론
흰가루병 병원균 생활사
밀의 흰가루병을 일으키는 병원균은 Blumeria graminis f. sp. tritici (Bgt)로 활물기생성(biotrophic)이면서 매우 기주 특이적(host specificity)이며 무성생식 단계에서는 분생포자(conidia, conidiospores)를 생성하고, 유성생식 단계에서는 자낭포자(ascospores)를 생성한다. 분생포자와 자낭포자 모두 표면에 수분이 있거나 습한 조건에서 발아하며 95-100% 습도, 10-22°C 온도와 적은 직사광선이 적합한 조건이다. 하지만 25°C 이상의 고온이 지속되면 생장을 멈춰 오히려 발생이 줄어든다(Beest et al. 2008, Jankovics et al. 2015). 분생포자는 온화한 겨울에도 번식이 가능하고, 무색의 단세포로 크기는 32-44×12-15 μm이다. 자낭구(cleistothecia)는 검은 갈색으로 거의 구형이며 크기는 130-280 μm으로 자낭은 장타원형으로 이른 봄에 자낭구 안에 무색의 단세포인 20-23×10-13 μm의 크기의 자낭포자를 만드는데, 이러한 분생포자와 자낭포자를 일차 접종원(primary inoculum)이라고 한다(Glawe 2008). 흰가루병 병원균은 생육 주기가 짧고 공기중에 퍼져 쉽게 전파되며 병원성이 높은 새로운 레이스(race) 발생도 쉽다. 포자가 잎에 떨어지면 2시간 안에 특수한 배아관(germ tube)이 신장해서 부착기(appressorium)를 만들어 잎, 엽초, 줄기와 이삭 등의 표피세포(epidermal cell)에 침투해서 영양분을 흡수하기 위한 원반형의 흡기(haustorium)를 만들고, 5일에서 8일이 지나서 분생포자가 만들어지는데 이를 2차 접종원(secondary inoculum)이라고 한다. 이러한 분생포자는 밀 재배기간 동안에 반복적으로 생장하고 번식하며 밀 생육에 피해를 준다(Chen et al. 2007, Kuckenberg et al. 2009, Walters et al. 2008, Wright et al. 1995). 무성생식이 끝나고 식물체 표면에 흰색의 고름주머니의 반점(pustules)이 생긴 후 점점 확대되어 원형 또는 타원형이 되고, 표면이 밀가루 뿌린 것과 비슷하게 된 후에 병반은 회색에서 담갈색으로 변하여 흑색의 작은 자낭구가 만들어진다(Fig. 1) (Acevedo-Garcia et al. 2017).
흰가루병이 밀 품질에 미치는 영향
Bgt는 감염후에 기주 식물의 양분을 흡수해서 이용하는데, 감염된 조직에서 모든 종류의 당분해효소인 invertase 활성이 증가해서 당을 Bgt에 공급하기 때문에 감염된 잎에서 종자로 전류 될 당이 줄어들고 뿌리의 생육이 억제되는 등 여러 생리적 활성이 억제된다(Deng et al. 2010, Sutton et al. 2007). Bgt는 감염 식물의 전분합성효소인 ADP-glucose pyrophosphorylase, α-1,4-phosphorylase나 sucrose synthase의 발현을 억제하기 때문에 종실의 전분합성이 줄고 이로 인해 수량 감소가 일어난다. 그리고 phosphoglycerate mutase, 3-phosphoglycerate kinase와 UTP-glucose-1-phosphate uridylyltransferase의 발현이 증가해서 해당작용(glycolysis)이 활발해지면서 전분 분해 및 소비를 촉진하게 된다(Gao et al. 2014b, Li et al. 2018). 단백질 생합성에 관련된 peptidylprolyl isomerase, cyclophilin A-2와 GTPase ObgE의 발현이 새롭게 나타나는데, 이런 현상은 종실 등숙 과정에서 단백질 함량이 증가하는 것과 유사해서 밀 품질과 밀접한 관련이 있는 triticin, serpin과 high molecular weight-glutenin subunit (HMW-GS)를 증가시키는 걸로 나타난다(Gao et al. 2014b, Li et al. 2018). 하지만 Bgt 감염에 의해 전분 및 단백질 합성 관련 효소의 활성 변화가 종실의 단백질 함량 및 질적 특성에 어떻게 얼마나 어떤 영향을 주는지에 대한 관련 연구는 진행중에 있다.
Bgt 방제에 사용되는 살균제는 트리아졸론(triazolone), 플푸트리아폴(flutriafol), 벤지미다졸(benzimidazole), 디니코나졸(diniconazole)과 티오카바메이트(thiocarbamate)가 사용되며 메톡시 아크릴레이트(methoxy acrylate)가 효과적이다. 그러나 같은 메톡시 아크릴레이트계인 메토미노스트로빈(metominostrobin)이나 피라메토스트로빈(pyrametostrobin)과 아족시스트로빈(azoxystrobin)의 동시 사용은 효과를 반감시키고, 프로피코나졸(propiconazole)과 플루시나졸(flusilazole)을 트리아졸론(triazolone)과 교대로 사용하면 밀 수량 감소를 막을 수 있다(Yang et al. 2013). 살균제를 종자에 처리하거나 엽면 살포를 하면 흰가루병을 감소시킬 수 있으며 종자소독과 엽면 살포를 같이 하면 방제 효율이 더 높아 진다(Christ & Frank 1989, Da Luz & Bergstrom 1986, Hardwick et al. 1994). 살균제를 과도하게 사용하거나 반복적인 사용은 종실의 단백질과 황(sulfur) 함량을 낮추어 빵 품질을 떨어드리고, 식품 안전성에도 치명적이기 때문에 적량을 처리해야 한다(Gao et al. 2018, Ruske et al. 2004).
규산염(silicate) 살포는 발병 부위의 과산화효소(peroxidase) 활성과 리그닌(lignin)을 증가시키고 포자 형성을 억제해서 Bgt이 퍼지는 것을 억제하는 효과가 있는 것으로 알려져 있다(Belanger et al. 2003, Delipoulos et al. 2010, Gao et al. 2018, Kanto et al. 2007). 최근 들어서는 생물학적 방제(biological control)에도 많은 연구가 이루어지고 있는데 보리 흰가루병 병원균을 미리 접종하면 밀 Bgt의 피해를 감소시킬 수 있으며(Curtis et al. 2012) 효모류인 Pseudozyma flocculosa도 Bgt의 효과적인 저해제로 작용한다(Jarvis et al. 2007). 효모류인 Rhodosporidium kratochvilovae, Cryptococcus laurentii나 Aureobasidium pullulans을 규산칼슘이나 황과 같이 사용하면 Bgt의 방제에 효과적이었고(Curtis et al. 2012), 생강(Zingiber officinale Roscoe)의 뿌리나 왕호장근(Reynoutria sacchaliensis L.)의 잎도 Bgt방제에 효과를 보였다(Vechet et al. 2009). 고초균(Bacillus subtilis)은 Bgt의 발아를 억제하고(Dunlap et al. 2011), 그람음성세균인 Sphingomonas는 병징을 완화시키는 걸로 알려져 있다(Wachowska et al. 2013).
우리나라에서는 4-5월경 비가 잦고 온도가 낮으면 발생하기 시작해서 수확기에 심하게 발생하는데, Bgt방제를 위해서는 적기 파종, 적당한 재식 밀도와 질소 시비, 윤작과 수확 후 Bgt에 감염된 밀 잔재물의 확실한 제거가 도움이 된다. 하지만 병을 일으키는 포자가 공기로 비산되기 때문에 Bgt방제에는 한계가 있다. 국내 Bgt 발생은 강수량과 포장의 과습 상태에 따른 발생이 연차간 지역 간에 차이가 있을 것으로 추정되지만 체계적인 예찰과 병 발생에 따른 수량 및 품질에 미치는 영향에 대한 평가는 이루어지지 않았다. 국내에서는 밀과 보리에 사용하는 흰가루병 살균제로 펜티오피라드(Penthiopyrad) 유제, 마이클로뷰타닐(Myclobutanil) 수화제와 아족시스트로빈 디메토모르프(azoxystrobin difenoconazole) 입상 수화제가 등록되어 있다.
흰가루병 병원균에 대한 면역 반응
최근 흰가루병 병원균 감염 경로에 대한 식물체의 면역 반응 및 기작에 대한 연구가 활발하게 진행되고 있다(Fig. 2). 식물은 세포 표면의 수용체를 통해 외부 신호를 감지하는데 세포 표면의 pattern recognition receptor (PRR)는 pathogen-associated molecular patterns (PAMP)를 인식하여 pattern-triggered immunity (PTI)를 활성화한다(Zhao et al. 2022). PTI 활성화는 이온 흐름변화, 활성산소종(reactive oxygen species, ROS) 생성, mitogen-activated protein kinase (MAPK) cascades 같은 하류(downstream) 신호전달로 이어진다(DeFalco & Zipfel 2021, Yu et al. 2017). 식물에서 밝혀진 PRR은 대부분이 원형질막에 위치한 receptor-like kinase (RLK)나 receptor-like protein (RLP) 계열에 속하며, RLK와 RLP는 ligand가 결합하는 N-말단 영역에 위치하는 extracellular domain (ectodomain, ECD)의 형태에 따라 leucine-rich repeat (LRR), lectin-like domain, cysteine-rich domain, lysine motif (LysM)와 epidermal growth factor (EGF)-like domain으로 분류된다(Lee et al. 2021, Sinha et al. 2022, Tang et al. 2017, Wu et al. 2013). RLK와 RLP의 ECD는 그에 맞는 ligand와 결합하고, 세포질 kinase domain은 인산화를 통해 세포 내로 신호를 전달하여 특정 리간드에 반응한다(Couto & Zipfel 2016, He et al. 2018b, Hohmann et al. 2017). RLP는 세포질의 kinase domain이 없기 때문에 외부 신호를 세포 내 신호로 변환하기 위해서 RLK와 상호작용을 한다(Fritz-Laylin et al. 2005, Mapuranga et al. 2022).
밀의 leucine-rich repeat (LRR)-RLK인 TaRLK1와 TaRLK2, 이배체 밀 Haynaldia villosa의 lectin type RLK (LecRK-V)와 malectin-like/LRR-RLK (RLK-V) 유전자는 곰팡이 결정인자(fungal determinants)를 인식하여 세포 내부로 신호를 전달하는데 관여하는 막단백질 조절을 통하여 Bgt 저항성을 조절하는 것으로 알려져 있다(Chen et al. 2016, Hu et al. 2018, Wang et al. 2018). TaRLK1와 TaRLK2를 과발현 시킨 계통은 감염 부위에 ROS를 증가시켜 Bgt에 대한 저항성이 증가하였다(Chen et al. 2016). LecRK-V매개 저항성은 ROS 및 SA 신호전달과 관련된 저항성 기작을 매개하는 것으로 알려져 있으며 LecRK-V 과발현체는 Bgt 흡기 형성 감소로 흰가루병 저항성이 증가하였다(Hu et al. 2018, Wang et al. 2018). RLK-V는 기본 저항성(basal defense)과 Pm21 매개 저항성을 조절하며 선택적 스플라이싱(alternative splicing)에 의해 온전한 형태의 RLK-V1.1과 잘린형태(truncated form)의 RLK-V1.2 두 가지 형태의 전사체를 가지며 RLK-V1.1이 ROS 축적 및 세포사멸을 유도하여 저항성 반응을 일으키는 것으로 알려져 있다(Hu et al. 2018, Wang et al. 2018).
식물호르몬인 자스몬산(Jasmonic acid, JA)과 에틸렌(ethylene, ET)의 신호 전달 경로는 병 관련 유전자들의 발현과 ROS 조절을 통해 Bgt에 대한 저항성에 관여한다(Cao et al. 2014, Jing et al. 2019, Li et al. 2017, Xu et al. 2016, Zhao et al. 2014). JA에 의해 유도된 basic helix-loop-helix (bHLH) 전사 인자인 TaMYC4는 Jasmonate-ZIM domain (JAZ) 유전자인 TaJAZ1 과 직접적인 상호작용을 통해 전사활성이 억제된다. TaJAZ1의 ZIM 도메인은 NOVEL INTERACTOR OF JAZ (MINJA)의 C-말단과 상호 작용하고 TaNINJA의 N-말단 EAR 모티프는 TOPLESS (TPL)와 상호작용하여 TaJAZ1-TaNINJA-TaTPL 전사공동억제자 복합체를 형성한다. Bgt 감염에 의해 JA가 축적되면 TaJAZ1을 분해하고 전사공동억제자 복합체 형성을 방해하여 TaPR유전자들의 발현과 ROS 축적을 억제한다(Jing et al. 2019). 그리고 RNA Polymerase Ⅱ (RNA Pol Ⅱ)는 TaMED25와 ETHYLENE INSENSITIVE3-LIKE1 (TaEIL1) 사이의 상호작용에 의해 ETHYLENE RESPONSE FACTOR 1 (TaERF1)의 전사를 상향조절하여 PR 유전자의 발현과 ROS의 축적을 억제한다(Liu et al. 2016).
다양한 탈아세틸화효소(histone deacetylase, HDAC)도 병원균 감염에 대한 식물 저항성에 양성 및 음성 조절자 역할을 한다(Ding & Wang 2015, Kong et al. 2020, Ramirez-Prado et al. 2018). Bgt 감염에 의해 히스톤 아세틸화효소(Histone acetyltransferase, HAT)가 증가되고, 히스톤 아세틸화효소가 히스톤의 라이신(Lys) 잔기에 아세틸기를 증가시키면 염색질(chromatin) 구조가 느슨해저 방어 관련 유전자의 발현이 촉진된다. 반면에 탈아세틸화효소에 의해 아세틸 그룹이 제거가 되면 염색질 구조가 긴밀해지면서 전사가 억제된다. 밀의 RPD3타입 탈아세틸화효소인 TaHDA6는 WD repeats (WDR) 단백질인 TaHOS15와 상호작용하여 히스톤의 탈아세틸화를 통해 방어 관련 유전자의 발현을 억제한다(Liu et al. 2019). 탈아세틸화효소 2 (HD2)의 구성원인 TaHDT701은 TaHDA6 및 TaHOS15와 상호작용하여 HDAC복합체를 형성하는데 이 HDAC복합체는 TaPR1, TaPR2, TaPR5 및 TaWRKY45와 같은 밀 방어 관련 유전자에서 히스톤 탈아세틸화를 매개하여 Bgt에 대한 방어 관련 유전자 전사 및 방어 반응을 억제한다.
Pm 저항성 유전자는 레이스 특이적(race-specific) 저항성과 레이스 비특이적(race-non-specific) 저항성 타입으로 나뉜다. 첫번째 레이스 특이적 저항성은 질적 저항성(qualitative resistance), 모든 식물 성장 단계 저항성(all stage resistance, ASR) 또는 단일유전자 저항성이라고도 부른다. 레이스 특이적 저항성은 Bgt에 대한 유전자 대 유전자 대응 방식(gene-for-gene manner)으로 관련된 단일 주동 유전자(major gene, R gene)에 의해서 저항성을 가지게 된다(Mapuranga et al. 2022, Maurya et al. 2021). Pm4a (MCTP-kinase), Pm24 (tandem kinase gene WTK3), Pm38 (ATP-binding cassette (ABC) transporter)과 Pm46 (hexose transporter)을 제외한 대부분의 흰가루병 저항성 유전자는 주로 Nucleotide binding site-Leucine rich Repeat (NLR) 형태의 수용체를 암호한다(Koller et al. 2018, Krattinger et al. 2009, Lu et al. 2020, Moore et al. 2015, Sanchez-Martín et al. 2021). 그러나 대부분의 레이스 특이적 저항성은 Bgt에 대한 내구성(durability)이 낮아 3-5년 지나면 새로운 레이스 출현으로 쉽게 저항성을 잃게 된다(Lillemo et al. 2010, Shamanin et al. 2019, Wang et al. 2005). 1980년대에 중국에서는 Pm8저항성 유전자를 포함하는 품종이 70%에 달하였으나 Pm8저항성이 무너졌고(Sheng et al. 1995), 현재 중국 일부지역에서는 단일Pm21 유전자의 대규모 빈번한 사용으로 저항성이 무너질 위기에 놓여 있다. 미중부지역에서는 Pm3a (Niewoehner & Leath 1998)와 Pm4a (Parks et al. 2008)가 몇 년을 넘기지 못했고, Pm17도 5년을 넘기지 못했다(Cowger et al. 2009, Cowger et al. 2018). 호주에서는 Pm4b, Pm7, Pm24와 Pm28이 4년을 넘기지 못했다(Golzar et al. 2016). 따라서 흰가루병에 대한 넓은 범위의 병원체 저항성을 가진 새로운 저항성 유전자의 탐색 및 품종개발이 필요하다.
감수성유전자(susceptibility genes, S gene)도 흰가루병 병원균 감염에 관여를 하는데, S gene를 비활성화하거나 knock-down 시키면 저항성이 생긴다(Appiano et al. 2015, Consonni et al. 2006, Pessina et al. 2016, Wang et al. 2014). 대표적인 S gene은 MLO (Mildew-Locus-O)이며, 많은 식물종에서 MLO의 기능상실 돌연변이(mlo)가 흰가루병에 대한 저항성을 유발한다(Büschges et al. 1997). MLO는 R 유전자와 달리 열성인 mlo가 저항성을 부여하지만(Jorgensen 1992) 밀에서는 자연 발생적인 mlo 유전자 돌연변이가 발견되지 않았다(Acevedo-Garcia et al. 2017). 3개의 보리 MLO 유사체 TaMLO-A1, TaMLO-B1과 TaMLO-D1이 각 5AL, 4BL과4DL 염색체에서 보고되었으며(Devoto et al. 2003, Gao et al. 2018, Varallyay et al. 2012) nucleotide와 단백질 수준에서 각 98%와 99%의 유사도를 보였고(Wang et al. 2014), 보리 MLO와는 88% 유사도를 보였다(Elliott et al. 2002). TaMLO-B1의 과발현으로 흰가루병에 대한 감수성이 높아질 뿐만 아니라 표면의 원반형의 흡기(haustorium)도 비정상적으로 증가하였다(Elliott et al. 2002). mlo 돌연변이는 의도치 않은 다면발현 효과(pleiotropic effects)로 인한 생장저하(growth penalty)를 유발하는데, 보리와 애기장대에서 mlo 돌연변이는 캘러스 축적(callose deposition) 및 세포사(cell death), 노화(senescence) 유발 등이 보고되었다(Consonni et al. 2006, Humphry et al. 2006, Piffanelli et al. 2004). 하지만 targeting induced local lesions in genomes (TILLING) 기술을 이용한 밀의 TaMLO 돌연변이체에서 Bgt 저항성을 보였으나 식물성장에 영향을 나타내지는 않았고 (Acevedo-Garcia et al. 2017), 밀의 A, B와 D 게놈의 TaMLO을 모두 knock-out 시킨 돌연변이체(Tamlo-aabbdd) 중에 Tamlo-R32는 흰가루병에 강한 저항성을 가지면서도 성장저하 및 생산량 감소를 나타내지 않았다(Wang et al. 2014). Tamlo-R32는 4B 염색체에서 MLO 유전자를 포함하여 앞쪽으로 304 kb 결실이 발생하면서 앞쪽에 있던 Tonoplast monosaccharide transporter 3 (TaTMT3B) 유전자의 발현이 증가하여 성장 및 생산량 저하를 상쇄시킨 것으로 보인다(Wang et al. 2014, Li et al. 2022). 이와 유사한 음성적 조절자(negative regulator)로 enhanced disease resistance 1 (EDR1)의 돌연변이는 흰가루병 뿐만 아니라 일반적인 저항성도 나타냈다(Huckelhoven 2005).
흰가루병 저항성 자원
캐나다 품종인 6배체 밀 Axminster (Pm1a) (Sears & Briggle 1969)에서 처음으로 보고된 이후에 많은 6배체 밀 저항성 자원들이 보고되었으며 현재까지 보고된 자원 중에 중국 자원이 가장 많다. 중국자원으로는 Ulka (Pm2a), KM2939 (Pm2b), Xiaobaidong (Pm5a), CI 10904 (Pm5d), Fuzhuang 30 (Pm5e), Chinese Spring (Pm11), 82-7241 (Pm23), Chiyacao (Pm24a), Baihulu (Pm24b), D57 (Pm45)과 Hongyanglazi (Pm47), 일본 자원으로는 Asosan (Pm3a), Norin 10 (Pm14)과 Norin 26 (Pm10, Pm15), 독일 자원으로는 Kolibri (Pm3d), Ibis (Pm5c), N14 (Pm9)과 Tabasco (Pm46), 러시아 자원으로는 Chul (Pm3b)과 GUS 122 (Pm3j), 호주 계통 W150 (Pm3e)과 RL6058 (Pm38)이 보고되었다. 그리고 멕시코 Sonora (Pm3c)와 Amber (Pm3f), 프랑스 Aristide (Pm3g), 네팔 N324 (Pm3i), 이탈리아 Virest (Pm1e), 에스토니아 Meri (Pm28), 노르웨이 Saar (Pm39)와 방글라데시 Hombar (Pm44) 자원도 보고 되었다(Alam et al. 2011, Briggle 1969, Gao et al. 2012, Hsam et al. 1998, Huang et al. 2000b, Huang et al. 2004, Li et al. 2014, Lillemo et al. 2008, Peusha et al. 2000, Schneider et al. 1991, Sears & Briggle 1969, Singrün et al. 2003, Sourdille et al. 1999, Spielmeyer et al. 2005, Tosa et al. 1987, Tosa et al. 1988, Tosa & Sakai 1990, Xiao et al. 2013, Xue et al. 2012). 그리고 국제 밀-옥수수 연구소(CIMMYT)에서 육성된 Francolin#1과 Quaiu#3 계통은 중국에서 분리한 Bgt에 APR저항성을 지닌 것으로 보고되었고, 미국 추파밀인 Knox 62, Massey와 Redcoat는 중도이상의 APR 유전자를 2-3개 지닌 것으로 알려져 있다. 특히 Knox 62는 20년 이상 APR효과를 지닌 품종으로 유명하다(Liu et al. 2001). 그리고 프랑스 추파밀인 RE714는 또다른 Bgt 저항성 유전자 powdery mildew resistance gene (MlRE)을 가지고 있는 것으로 보고되었다(Chantret et al. 1999, Das & Griffey 1994, Ren et al. 2017). 3개의 APR유전자 Pm38 (Lr34/Yr18/Pm38/Sr57), Pm39 (Lr46/Yr29/Pm39/Sr58)와 Pm46 (Lr67/Yr46/Pm46/Sr55)를 지닌 계통이나 자원은 전세계적으로 유용하게 이용되고 있으며, 중국의 경우 CIMMYT의 유용자원을 활용한 shuttle breeding을 통해서 흰가루병과 녹병에 저항성인 08RC2525 (Chuanmai 32*2/Chapio), 07RC3941 (SW119*2/Tukuru)과 07RC3929 (SW119*2/Tukuru)를 육성하였다(Li et al. 2014).
염색체별로 보면 염색체 1A에는 T. militinae으로부터 유래한 유전자와 QTL 영역이 포함되어 있으며 염색체 2A의 QTL 부위는 다양한 야생밀 자원(T. monococcum, T. dicoccum, T. timopheevii, T. carthilicum)의 유전자와 QTL이 도입된 영역을 포함한다. 이러한 도입은 염색체 2B (T. carthlicum, T. dicoccoides), 5A (T. monococcum, T. militinae), 5B (T. dicoccoides)와 6B (T. timopheevi, T. dicoccoides, Ae. speltoides)에서도 나타난다(Jakobson et al. 2012, Marone et al. 2013).
현재까지 100여개가 넘는 APR QTL이 보고되었는데 APR QTL은 완전히 감염이 없는 저항성이 아니라 생육 기간에 Bgt 감염의 최소화를 의미하며 레이스 특이적 저항성을 포함하여 여러가지 유전자가 관여하는 양적인 의미의 저항성으로 이해해야 한다(Burdon et al. 2014, Li et al. 2014, Poland et al. 2009). APR QTL은 R 유전자 보다 Bgt 저항성에 내구성이 높지만 감염력이 높은 경우에는 QTL의 효과는 낮아진다. 따라서 흰가루병 발병이 심한 경우에는 R 유전자가 효과적이고 중간 이하의 발병에서는 APR QTL이 효과적이다(Gao et al. 2018, Kang et al. 2020, Li et al. 2014, Liu et al. 2001, Mundt 2014, Mwale et al. 2014, Shah et al. 2018, Tang et al. 2018). CIMMYT의 Francolin#1과 Quaiu#3의 recombinant inbred line (RIL) 집단에서 6개의 QTL (QPm.heau-1BL (Pm39), QPm.heau-1DL, QPm.heau-2DL, QPm.heau-4BL, QPm.heau-5BL, QPm.heau-6BS)이 보고되었는데 QPm.heau-1DL은 새롭게 보고된 것이고, QPm.heau-1BL (Pm39)과 QPm.heau-2DL은 Yr54과 같은 위치에 있으며 다면발현 저항성 유전자인 APR QTL이다(Ren et al. 2017). 중국 계통인 Zhou8425B에서 4개의 Bgt 저항성 QTL로 전체 Bgt 저항성의 27%를 설명할 수 있었고, 이들 4개 QTLs중에서 QPm.caas-3BS는 녹병 유전자인 QLr.hebau-3BS와 같은 위치에 있는 새로운 APR QTL이다(Jia et al. 2018, Zhang et al. 2017a). APR QTL는 1AS, 1AL, 2AS, 2AL, 3AS, 4AL, 5AL와 5BS에 각각 8개씩으로 많았고, 16개 APR QTL는 잎 녹병과 흰가루병에 동시에 저항성이었으며 11개 유전자좌는 잎 녹병, 줄 녹병과 흰가루병에 저항성이었다(Table 2, Fig. 3). 중국 계통 Bainong 64에서 보고된 QPm.caas-1AL과 QPm.caas-4DL은 흰가루병의 발병 심도를 낮추는 것과 상관이 있었으며 QPm.caas-3BS는 녹병 QTL인 QLr.hebau-3BS과 같은 위치인 것으로 보아 흰가루병과 녹병에 동시에 저항성 인 것으로 추정된다(Bai et al. 2012, Zhang et al. 2017a). Genome-wide association mapping (GWAS)나 연관 맵핑(linkage mapping)을 통해서 중간 정도의 발병에서는 4-5 QTL를 가진 품종이나 계통이 흰가루병에 저항성을 가지는 것으로 나타났다(Asad et al. 2012, Jia et al. 2018). 보리에서는 과산화효소 유전자군(peroxidase gene family)이 Bgt와 녹병에 저항성인 것으로 알려져 있는데, 밀에서도 이와 유사할 가능성이 높기 때문에 관련 유전자에 대한 연구가 이루어지고 있다(Gonzalez et al. 2010).
형질전환 및 유전자 교정을 통한 흰가루병 저항성 식물체 개발 동향
6배체 밀의 높은 배수성, 큰 게놈 사이즈(17 Gb)와 전이 요소(transposable elements)를 포함하는 반복 시퀀스 함량(80-90%)은 정방향(forward) 및 역방향(reverse) 유전분석을 어렵게 할 뿐만 아니라 virus-induced gene silencing (VIGS) 및 RNA interference (RNAi)과 같은 일부 형질전환 방법으로 형질전환 식물체를 얻는 데에도 어려움이 있다(Slade et al. 2005, Unniyampurath et al. 2016). 그러나 최근 clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated 9 (Cas9) 등 유전자 교정 기술의 급속한 발전으로 특정 유전자에 대한 돌연변이 유발이 기능해졌고 흰가루병 저항성 밀을 생성하기 위한 감수성 유전자를 제거하는 데에도 사용되었다(Kim et al. 2015, Lamichhane & Thapa 2022, Shan et al. 2013, Upadhyay et al. 2013, Wang et al. 2014, Zhang et al. 2016). ERD1이 knock-down 된 Taedr1 RNAi 식물체는 잎에서 대조군보다 현저히 적은 분생포자를 보였으며 H2O2 축적과 callose 침착이 유도되었다(Zhang et al. 2017b). 그리고 CRISPR/Cas9 기술로 유전자 편집한 Taedr1식물체에서도 곰팡이에 의해서 유발되는 세포 사멸과 상관없는 Bgt에 저항성을 보였다(Zhang et al. 2017b). 유사하게 TaMLO 상동체의 VIGS 의한 RNAi silencing은 흰가루병 저항성을 보인 것과 마찬가지로(Varallyay et al. 2012) CRISPR/Cas9기술로 TaMLO-A1 대립유전자의 유전자 편집 된 식물체도 흰가루병 저항성이 증가하였다(Wang et al. 2014). Jas 모티프가 결여된 TaJAZ1 단백질을 과발현하는 형질전환 밀 계통에서 microcolony 형성이 감소하고, TaPR1/2 유전자 발현 및 ROS 축적이 증가하여 흰가루병에 대한 저항성이 증가되었다(Jing et al. 2019). 그래서 TaJAZ1 유전자의 Jas 모티프를 CRISPR/Cas9와 같은 게놈 편집 기술로 교정하면 흰가루병 저항성이 증가한 식물체를 생성할 가능성이 높을 것으로 제시되었다(Jing et al. 2019).
결 론
밀은 흰가루병에 의해 수량 감소뿐만 아니라 전분 및 단백질 함량과 밀가루 품질에도 영향을 받는데 품종이나 발병시기 및 평가 방법에 따른 차이가 크다. Bgt방제를 위해서는 적기 파종, 적당한 재식 밀도와 질소 시비, 윤작과 수확 후 Bgt에 감염된 밀 잔재물의 확실한 제거와 적정한 살균제 처리 등이 도움이 된다. 하지만 병을 일으키는 포자가 공기로 비산되기 때문에 Bgt방제에 한계가 있고 병원성이 높은 새로운 레이스 발생도 쉽다. 현재까지 많은 저항성 유전자(Pm gene)가 알려져 있지만 클로닝된 유전자는 몇 개 되지 않으며 이들 저항성 유전자들의 대부분은 레이스 특이적인 유전자로 Bgt에 대한 내구성이 낮아 3-5년 지나면 새로운 레이스 출현으로 쉽게 저항성을 잃게 된다. 따라서 흰가루병에 대한 넓은 범위의 병원체 저항성을 가진 새로운 저항성 유전자의 지속적인 탐색 및 품종개발이 필요하다. 우리나라에서는 4-5월경 비가 잦고 온도가 낮으면 발생하기 시작해서 수확기에 심하게 발생하는데 흰가루병 발생에 대한 체계적인 예찰이나 흰가루병 발생에 따른 수량 및 품질의 영향에 대한 평가는 제대로 이루어진 적이 없는 실정이다. 따라서 국산 밀 안정적 공급과 국내환경에 맞는 저항성 품종 육성을 위해 먼저 정밀 검정체계 구축을 통한 표현형 데이터 획득이 필요하다. 그리고 효율적인 분자 마커 개발을 위해 genome-wide association mapping (GWAS)와 Genomic selection (GS) 분석으로 QTL 및 유전자 선별 등 marker-associated selection (MAS) 연구를 통해 국내환경에 맞는 품종개발 및 선발 마커 개발이 이루어져야 한다. 또한 면역체계의 신호전달 연구와 수량이나 농업형질의 피해 없이 저항성을 증진한 유전자의 유전자 편집을 통한 저항성 증진 연구도 함께 이루어져야 한다.
적 요
흰가루병(Blumeria graminis f. sp. tritici)은 밀 생산에 상당한 경제적 손실을 초래한다. 수십 년 동안 밀 흰가루병에 대한 식물 저항성이 조사되었으며 많은 저항성 유전자 및 양적 형질 유전자좌(QTL)를 발견하였다. 국내에서는 4-5월경 비가 잦고 온도가 낮으면 발생하기 시작해서 수확기에 심하게 발생하며 수확량, 단백질 함량 및 밀가루 품질에도 영향을 준다. 그러나 국내에서는 흰가루병 발생에 대한 체계적인 예찰이나 흰가루병 발생에 따른 수량 및 품질의 영향에 대한 평가도 제대로 이루어진 적이 없다. 본 연구에서는 흰가루병에 대한 이해와 보고된 저항성 유전자, QTL 및 유전자 마커에 대한 최근 연구 동향을 정리하여 국내에 맞는 저항성 품종 개발과 선별 마커 개발에 도움이 되고자 하였다.
사 사
본 연구는 2023년도 농촌진흥청 국립식량과학원 전문연구원 과정 지원사업과 농촌진흥청 연구사업(과제명: 가공 용도별 밀 품종개발 및 육종효율 증진연구(4단계), 과제번호: PJ 016771012023)에 의해 이루어진 것임.
Fig. 1
Wheat powdery mildew (Blumeria graminis f. sp. tritici) life cycle.
Fig. 2
Schematic representation of wheat defense responses to Bgt infection from Mapuranga et al. (2022). ABA, abscisic acid; ET, ethylene; ETI, effector-triggered immunity; ETS, effector-triggered susceptibility; HAT, histone acetyltransferase; JA, Jasmonate; PR, pathogenesis-related; PRR, pattern recognition receptor; PTI, PAMP-triggered immunity; ROS, reactive oxygen species.
Fig. 3
Projection of wheat Pm genes (in bold) and QTL (blue bars) onto wheat chromosomes, grey section on each chromosome represents centromere. The positions of these genes and QTL are estimated from their flanking molecular markers from previous publications in integrated map (Maccaferri et al. 2015) and from Kang et al. (2020). For those with either flanking marker or close marker not available, are excluded from map. Some Pm genes which are placed at the same position, only one gene randomly chosen to be present, the number of other genes in this case is given in bracket after.
Table 1
Genes associated with powdery mildew resistance, their chromosomal location, cultivar/line, source and molecular markers modified from Kang et al. (2020).
Summary of quantitative trait loci (QTLs) for adult-plant resistance to powdery mildew in wheat (Triticum aestivum L.) modified from Li et al. (2014) and Kang et al. (2020).
Table 2
QTLs
Chromosome
Marker interval
R2z
QPm.caas-1AL
1AL
Xbarc148-Xwmc550
7.4-9.9%
QPm.crag-1A
1AL
Xcdo572-Xbad442
39.3-43.0%
QPm.sfr-1A
1AL
Xpsr1201b-Xpsr941
7.7%
QPm.caas-1AS
1AS
Xgdm33-Xpsp2999
19.9-26.6%
QPm.osu-1A
1AS
Pm3a
63.0%
Qaprpm.cgb-1B
1B
WMC269.2-CWM90
4.8-20.3%
Qaprpm.cgb-1B
1B
P4133-170-Xgwm582
4.8%
QPm.caas-1BL.1
1BL
IWB72835-IWB18787
7.2%
QPm.osu-1B
1BL
WMC134
14.0%
QPm.vt-1B
1BL
WG241
17.0%
QPm.vt-1BL
1BL
Xgwm259-Xbarc80
15.0%-17.0%
QPm.sfr-1B
1BS
CD9b-Xpsr593a
11.6%
QPm.ttu-1B
1BS
Xgwm3000
4.0-5.0%
QPm.heau-1DL
1DL
wPt-5721-wPt-1865
6.1-8.5%
QPm.sfr-1D
1DL
Xpsr168-Xglk558b
9.5%
QPm.inra-1D.1
1DS
Xgwm106
12.6%
Qpm.sdau-2A
2A
cfa2263-D-1395795
8.6-9%
QPm.crag-2A
2AL
Pm4b-gbxG303
22.7-39.2%
QPm.ttu-2A
2AL
Xgwm311-Xgwm382
5.0%
QPm.vt-2A
2AL
Xgwm304-Xgwm294
26.0-29.0%
QPm.vt-2AL
2AL
Xgwm304a-Xgwm312
29.0%
QPm.inra-2A
2AS
Xgwm275
7.4%
QPm.sfr-2A
2AS
Xpsr380-Xglk293b
7.7%
Qaprpm.cgb-2B
2B
Xwmc477-Xwmc272
5.4%
QPm.sdau-2B
2B
D-1054006—D-1114401
12.6-13.4%
QPm.caas-2B
2BL
Xgwm877.1-Xgwm435.1
5.7-8.0%
QPm.caas-2BL
2BL
Xbarc1139-Xgwm47
5.2-10.1%
QPm.inra-2B
2BL
Xrtp114R-Xcfd267b
10.3-36.3%
QPm.vt-2B
2BL
WG338-Xgwm526a
11.0%
QPm.vt-2BL
2BL
Xgwm501-Xgwm191
11.0-15.0%
QPm.caas-2BS
2BS
Xbarc98-Xbarc1147
10.6-20.6%
QPm.crag-2B
2BS
Xgwm148-gbxG553
23.6-71.5%
QPm.umb-2BS
2BS
wPt-9402
3.9-13.0%
QPm.umb-2BS
2BS
Xgwm410b-Xgwm148
8.0-10.2%
QPm.caas-2DL
2DL
Xwmc18-Xcfd233
5.7-11.6%
QPm.ipk-2D
2DL
Xglk558-XksuD23
unknown
QPm.sfr-2D
2DL
Xpsr932-Xpsr331a
10.0%
QPm.umb-2DL
2DL
Xwmc167-Xgwm301
4.3-9.5%
QPm.caas-2DS
2DS
Xcfd51-Xcfd56
2.3-3.4%
QPm.inra-2D-a
2DS
Xgwm102
19.0%
QPm.inra-2D-b
2DS
Xcfd2e
16.5%
Qaprpm.cgb-3A
3A
Xwmc21-Xwmc505.2
9.8%
QPm.crag-3A
3AS
Xpsr598-Xgwm5
21.4-25.9%
QPm.nuls-3AS
3AS
Xstm844tcac-Xbarc310
8.1-20.7%
QPm.sfr-3A
3AS
Xpsr598-Xpsr570
10.4%
Qaprpm.cgb-3BL
3B
Xgwm181-Xgwm340
13.3%
QPm.caas-3B
3BS
XksuG53-Xfba190
7.3%
QPm.caas-3BS
3BS
IWB21064-IWB64002
7.1%
QPm.inra-3B
3BS
Xgwm389
22.7%
QPm.osu-3B
3BS
WMS533
10.0%
QPm.inra-3D
3DS
Xcfd152, Xgwm707
9.3-15.2%
QPm.sfr-3D
3DS
Xpsr1196a-Lrk10-6
15.7%
QPm.tut-4A
4A
Xwmc232-Xrga3.1
24.0-46.0%
QPm.crag-4A.
4AL
XgbxG036-XgbxG542
22.3%
QPm.inra-4A
4AL
XgbxG036
4.9-6.9%
QPm.osu-4A
4AL
WMS160
12.0%
QPm.sfr-4A.1
4AL
Xgwm111c-Xpsr934a
14.7%
QPm.sfr-4A.2
4AL
Xmwg710b-Xglk128
14.3%
QPm.ttu-4A
4AL
Xwmc232-Xgwm160
35.0-54.0%
QPm.caas-4BL
4BL
Xgwm375-Xgwm251
5.9%
QPm.Caas-4BL.1
4BL
Xgwm149-Xgwm495
9.1-14.7%
QPm.caas-4BL.2
4BL
IWB35851-IWB60096
8.8%
QPm.ipk-4B
4BL
Xcdo795-Xbcd1262
Unknown
QPm.nuls-4BL
4BL
XwPt1505-Xgwm149
21.0-40.2%
QPm.sfr-4B
4BL
Xpsr593b-Xpsr1112
7.5%
QPm.caas-4DL
4DL
Xbarc200-Xwmc33
15.2-22.7%
QPm.sfr-4D
4DL
Xglk302b-Xpsr1101a
14.4%
Qaprpm.cgb-5A
5A
P3616-185-P3616-195
13.2%
QPm.tut-5A
5A
Xgwm666-Xcfd30-Xbarc319
14.0-16.0%
QPm.nau-5AL
5AL
Xcfd39/Xmag1491-Xmag1493
59.0%
QPm.nuls-5A
5AL
Xgwm617b-Xwmc327
4.2-15.2%
QPm.sfr-5A.2
5AL
Xpsr1194-Xpsr918b
16.6%
QPm.sfr-5A.3
5AL
Xpsr911-Xpsr120a
10.5%
QPm.umb-5AL
5AL
wPt-2426
4.0-9.7%
QPm.sfr-5A.1
5AS
Xpsr644a-Xpsr945a
22.9%
QPm.ttu-5A
5AS
Xgwm186-Xgwm415
4.0-6.0%
Qaprpm.cgb-5B
5B
Xgwm213-Xgwm499
19.8%
QPm.inra-5B.2
5BL
Xgwm790b
11.1%
QPm.sfr-5B
5BL
Xpsr580b-Xpsr143
12.6%
QPm.nuls-5B
5BS
Xbarc4-Xgwm274b
9.7%
QPm.ttu-5B
5BS
Xgwm133.mi6-Xgwm205.mi1
4.0-6.0%
QPm.umb-5BS
5BS
wPt-1261
3.1%
QPm.umb-5BS
5BS
Xbarc128a-Xgwm213
8.1-12.9%
QPm.caas-5D
5D
Xmwg922-Xbcd1103
5.9%
QPm.crag-5D.1
5DL
Xgwm639a-Xgwm174
30.2-38.9%
QPm.crag-5D.2
5DL
Xcfd8B9-Xcfd4A6
24.0-37.8%
QPm.inra-5D.1
5DL
Xcfd26
28.1-37.7%
QPm.inra-5D.2
5DL
XgbxG083c
37.7%
QPmVpn.inra-5D
5DL
Xcfd8
11.0%
QPm.inra-5D
5DS
cfd189
9.0%
QPm.crag-6A
6AL
MlRE
19.8-53.9%
QPm.inra-6A
6AL
MIRE(Xgwm427)
8.8-13.4%
Qaprpm.cgb-6B
6B
Xgwm193-P3470-210
21.0%
QPm.caas-6BL.1
6BL
Xgwm219-Xbarc24
2.5-5.2%
QPm.caas-6BL.2
6BL
Xbarc24-Xbarc345
0.5-1.9%
QPm.caas-6BS
6BS
Xbarc79-Xgwm518
10.3-16.0%
QPm.sfr-6B
6BS
Xpsr167b-Xpsr964
8.7%
QPm.umb-6BS
6BS
wPt-6437-Xwmc494
6.5-10.3%
QPm.osu-6D
6DS
BARC196
5.0%
Qaprpm.cgb-7A
7A
CWM462.2-Xgwm635.2
8.0%
Qaprpm.cgb-7A
7A
Xgwm282-P1111-202
15.7%
QPm.tut-7A
7A
Xgwm635-Xbarc70-Waxy
9.0-28.0%
QPm.umb-7AL
7AL
Xgwm428-Xcfa2040
6.4-13%
QPm.caas-7A
7AS
Xbarc127-Xbarc174
6.3-7.1%
QPm.inra-7A
7AS
Xfba069-Xgwm344
2.9-6.4%
Qaprpm.cgb-7B
7B
Xwmc273-Xwmc276
12.6%
QPm.crag-7B
7BL
XpdaC01-XgbxR035b
22.8-33.5%
QPm.inra-7B
7BL
Xgwm577
1.7%
QPm.nuls-7BL
7BL
Xwmc581-XwPt8007
4.90%
QPm.sfr-7B.1
7BL
Xpsr593c-Xpsr129c
11.3%
QPm.sfr-7B.2
7BL
Xglk750-Xmwg710a
31.8%
Qaprpm.cgb-7D
7D
Xwmc436-Xgwm44
3.8-4.6%
Qaprpm.cgb-7D
7D
Xgdm88-WMC463
14.20%
QPm.caas-7D
7D
Xwg834-Xbcd1438
29.6%
QPm.caas-7DS
7DS
XcsLV34-Xgwm295
7.6-13.8%
QPm.caas-7DS
7DS
IWB41108-IWB53819
4.21%
QPm.caas-7DS
7DS
Ltn-Xgwm295.1
12.0%
QPm.inra-7D.1
7DS
Xgpw1106
10.6%
QPm.ipk-7D
7DS
Xwg834-Xbcd1872
Unknown
zR2, percentage of variance explained by the QTL.
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Current Trends in Wheat Breeding Strategies for Developing Domestic Wheat Cultivars in Korea Hajeong Kang, Hyoun-Min Park, San-Gu Lee, Eun-Ha Kim, Muhammad Imran, Hanyoung Choi, Myeong-Ji Kim, Seonwoo Oh Korean Journal of Breeding Science.2024; 56(4): 491. CrossRef
Research Advances in Wheat Breeding and Genetics for Powdery Mildew Resistance
Fig. 1
Wheat powdery mildew (Blumeria graminis f. sp. tritici) life cycle.
Fig. 2
Schematic representation of wheat defense responses to Bgt infection from Mapuranga et al. (2022). ABA, abscisic acid; ET, ethylene; ETI, effector-triggered immunity; ETS, effector-triggered susceptibility; HAT, histone acetyltransferase; JA, Jasmonate; PR, pathogenesis-related; PRR, pattern recognition receptor; PTI, PAMP-triggered immunity; ROS, reactive oxygen species.
Fig. 3
Projection of wheat Pm genes (in bold) and QTL (blue bars) onto wheat chromosomes, grey section on each chromosome represents centromere. The positions of these genes and QTL are estimated from their flanking molecular markers from previous publications in integrated map (Maccaferri et al. 2015) and from Kang et al. (2020). For those with either flanking marker or close marker not available, are excluded from map. Some Pm genes which are placed at the same position, only one gene randomly chosen to be present, the number of other genes in this case is given in bracket after.
Fig. 1
Fig. 2
Fig. 3
Research Advances in Wheat Breeding and Genetics for Powdery Mildew Resistance
Genes associated with powdery mildew resistance, their chromosomal location, cultivar/line, source and molecular markers modified from Kang et al. (2020).
Summary of quantitative trait loci (QTLs) for adult-plant resistance to powdery mildew in wheat (Triticum aestivum L.) modified from Li et al. (2014) and Kang et al. (2020).
QTLs
Chromosome
Marker interval
R2z
QPm.caas-1AL
1AL
Xbarc148-Xwmc550
7.4-9.9%
QPm.crag-1A
1AL
Xcdo572-Xbad442
39.3-43.0%
QPm.sfr-1A
1AL
Xpsr1201b-Xpsr941
7.7%
QPm.caas-1AS
1AS
Xgdm33-Xpsp2999
19.9-26.6%
QPm.osu-1A
1AS
Pm3a
63.0%
Qaprpm.cgb-1B
1B
WMC269.2-CWM90
4.8-20.3%
Qaprpm.cgb-1B
1B
P4133-170-Xgwm582
4.8%
QPm.caas-1BL.1
1BL
IWB72835-IWB18787
7.2%
QPm.osu-1B
1BL
WMC134
14.0%
QPm.vt-1B
1BL
WG241
17.0%
QPm.vt-1BL
1BL
Xgwm259-Xbarc80
15.0%-17.0%
QPm.sfr-1B
1BS
CD9b-Xpsr593a
11.6%
QPm.ttu-1B
1BS
Xgwm3000
4.0-5.0%
QPm.heau-1DL
1DL
wPt-5721-wPt-1865
6.1-8.5%
QPm.sfr-1D
1DL
Xpsr168-Xglk558b
9.5%
QPm.inra-1D.1
1DS
Xgwm106
12.6%
Qpm.sdau-2A
2A
cfa2263-D-1395795
8.6-9%
QPm.crag-2A
2AL
Pm4b-gbxG303
22.7-39.2%
QPm.ttu-2A
2AL
Xgwm311-Xgwm382
5.0%
QPm.vt-2A
2AL
Xgwm304-Xgwm294
26.0-29.0%
QPm.vt-2AL
2AL
Xgwm304a-Xgwm312
29.0%
QPm.inra-2A
2AS
Xgwm275
7.4%
QPm.sfr-2A
2AS
Xpsr380-Xglk293b
7.7%
Qaprpm.cgb-2B
2B
Xwmc477-Xwmc272
5.4%
QPm.sdau-2B
2B
D-1054006—D-1114401
12.6-13.4%
QPm.caas-2B
2BL
Xgwm877.1-Xgwm435.1
5.7-8.0%
QPm.caas-2BL
2BL
Xbarc1139-Xgwm47
5.2-10.1%
QPm.inra-2B
2BL
Xrtp114R-Xcfd267b
10.3-36.3%
QPm.vt-2B
2BL
WG338-Xgwm526a
11.0%
QPm.vt-2BL
2BL
Xgwm501-Xgwm191
11.0-15.0%
QPm.caas-2BS
2BS
Xbarc98-Xbarc1147
10.6-20.6%
QPm.crag-2B
2BS
Xgwm148-gbxG553
23.6-71.5%
QPm.umb-2BS
2BS
wPt-9402
3.9-13.0%
QPm.umb-2BS
2BS
Xgwm410b-Xgwm148
8.0-10.2%
QPm.caas-2DL
2DL
Xwmc18-Xcfd233
5.7-11.6%
QPm.ipk-2D
2DL
Xglk558-XksuD23
unknown
QPm.sfr-2D
2DL
Xpsr932-Xpsr331a
10.0%
QPm.umb-2DL
2DL
Xwmc167-Xgwm301
4.3-9.5%
QPm.caas-2DS
2DS
Xcfd51-Xcfd56
2.3-3.4%
QPm.inra-2D-a
2DS
Xgwm102
19.0%
QPm.inra-2D-b
2DS
Xcfd2e
16.5%
Qaprpm.cgb-3A
3A
Xwmc21-Xwmc505.2
9.8%
QPm.crag-3A
3AS
Xpsr598-Xgwm5
21.4-25.9%
QPm.nuls-3AS
3AS
Xstm844tcac-Xbarc310
8.1-20.7%
QPm.sfr-3A
3AS
Xpsr598-Xpsr570
10.4%
Qaprpm.cgb-3BL
3B
Xgwm181-Xgwm340
13.3%
QPm.caas-3B
3BS
XksuG53-Xfba190
7.3%
QPm.caas-3BS
3BS
IWB21064-IWB64002
7.1%
QPm.inra-3B
3BS
Xgwm389
22.7%
QPm.osu-3B
3BS
WMS533
10.0%
QPm.inra-3D
3DS
Xcfd152, Xgwm707
9.3-15.2%
QPm.sfr-3D
3DS
Xpsr1196a-Lrk10-6
15.7%
QPm.tut-4A
4A
Xwmc232-Xrga3.1
24.0-46.0%
QPm.crag-4A.
4AL
XgbxG036-XgbxG542
22.3%
QPm.inra-4A
4AL
XgbxG036
4.9-6.9%
QPm.osu-4A
4AL
WMS160
12.0%
QPm.sfr-4A.1
4AL
Xgwm111c-Xpsr934a
14.7%
QPm.sfr-4A.2
4AL
Xmwg710b-Xglk128
14.3%
QPm.ttu-4A
4AL
Xwmc232-Xgwm160
35.0-54.0%
QPm.caas-4BL
4BL
Xgwm375-Xgwm251
5.9%
QPm.Caas-4BL.1
4BL
Xgwm149-Xgwm495
9.1-14.7%
QPm.caas-4BL.2
4BL
IWB35851-IWB60096
8.8%
QPm.ipk-4B
4BL
Xcdo795-Xbcd1262
Unknown
QPm.nuls-4BL
4BL
XwPt1505-Xgwm149
21.0-40.2%
QPm.sfr-4B
4BL
Xpsr593b-Xpsr1112
7.5%
QPm.caas-4DL
4DL
Xbarc200-Xwmc33
15.2-22.7%
QPm.sfr-4D
4DL
Xglk302b-Xpsr1101a
14.4%
Qaprpm.cgb-5A
5A
P3616-185-P3616-195
13.2%
QPm.tut-5A
5A
Xgwm666-Xcfd30-Xbarc319
14.0-16.0%
QPm.nau-5AL
5AL
Xcfd39/Xmag1491-Xmag1493
59.0%
QPm.nuls-5A
5AL
Xgwm617b-Xwmc327
4.2-15.2%
QPm.sfr-5A.2
5AL
Xpsr1194-Xpsr918b
16.6%
QPm.sfr-5A.3
5AL
Xpsr911-Xpsr120a
10.5%
QPm.umb-5AL
5AL
wPt-2426
4.0-9.7%
QPm.sfr-5A.1
5AS
Xpsr644a-Xpsr945a
22.9%
QPm.ttu-5A
5AS
Xgwm186-Xgwm415
4.0-6.0%
Qaprpm.cgb-5B
5B
Xgwm213-Xgwm499
19.8%
QPm.inra-5B.2
5BL
Xgwm790b
11.1%
QPm.sfr-5B
5BL
Xpsr580b-Xpsr143
12.6%
QPm.nuls-5B
5BS
Xbarc4-Xgwm274b
9.7%
QPm.ttu-5B
5BS
Xgwm133.mi6-Xgwm205.mi1
4.0-6.0%
QPm.umb-5BS
5BS
wPt-1261
3.1%
QPm.umb-5BS
5BS
Xbarc128a-Xgwm213
8.1-12.9%
QPm.caas-5D
5D
Xmwg922-Xbcd1103
5.9%
QPm.crag-5D.1
5DL
Xgwm639a-Xgwm174
30.2-38.9%
QPm.crag-5D.2
5DL
Xcfd8B9-Xcfd4A6
24.0-37.8%
QPm.inra-5D.1
5DL
Xcfd26
28.1-37.7%
QPm.inra-5D.2
5DL
XgbxG083c
37.7%
QPmVpn.inra-5D
5DL
Xcfd8
11.0%
QPm.inra-5D
5DS
cfd189
9.0%
QPm.crag-6A
6AL
MlRE
19.8-53.9%
QPm.inra-6A
6AL
MIRE(Xgwm427)
8.8-13.4%
Qaprpm.cgb-6B
6B
Xgwm193-P3470-210
21.0%
QPm.caas-6BL.1
6BL
Xgwm219-Xbarc24
2.5-5.2%
QPm.caas-6BL.2
6BL
Xbarc24-Xbarc345
0.5-1.9%
QPm.caas-6BS
6BS
Xbarc79-Xgwm518
10.3-16.0%
QPm.sfr-6B
6BS
Xpsr167b-Xpsr964
8.7%
QPm.umb-6BS
6BS
wPt-6437-Xwmc494
6.5-10.3%
QPm.osu-6D
6DS
BARC196
5.0%
Qaprpm.cgb-7A
7A
CWM462.2-Xgwm635.2
8.0%
Qaprpm.cgb-7A
7A
Xgwm282-P1111-202
15.7%
QPm.tut-7A
7A
Xgwm635-Xbarc70-Waxy
9.0-28.0%
QPm.umb-7AL
7AL
Xgwm428-Xcfa2040
6.4-13%
QPm.caas-7A
7AS
Xbarc127-Xbarc174
6.3-7.1%
QPm.inra-7A
7AS
Xfba069-Xgwm344
2.9-6.4%
Qaprpm.cgb-7B
7B
Xwmc273-Xwmc276
12.6%
QPm.crag-7B
7BL
XpdaC01-XgbxR035b
22.8-33.5%
QPm.inra-7B
7BL
Xgwm577
1.7%
QPm.nuls-7BL
7BL
Xwmc581-XwPt8007
4.90%
QPm.sfr-7B.1
7BL
Xpsr593c-Xpsr129c
11.3%
QPm.sfr-7B.2
7BL
Xglk750-Xmwg710a
31.8%
Qaprpm.cgb-7D
7D
Xwmc436-Xgwm44
3.8-4.6%
Qaprpm.cgb-7D
7D
Xgdm88-WMC463
14.20%
QPm.caas-7D
7D
Xwg834-Xbcd1438
29.6%
QPm.caas-7DS
7DS
XcsLV34-Xgwm295
7.6-13.8%
QPm.caas-7DS
7DS
IWB41108-IWB53819
4.21%
QPm.caas-7DS
7DS
Ltn-Xgwm295.1
12.0%
QPm.inra-7D.1
7DS
Xgpw1106
10.6%
QPm.ipk-7D
7DS
Xwg834-Xbcd1872
Unknown
Table 1
Genes associated with powdery mildew resistance, their chromosomal location, cultivar/line, source and molecular markers modified from Kang et al. (2020).
Table 2
Summary of quantitative trait loci (QTLs) for adult-plant resistance to powdery mildew in wheat (Triticum aestivum L.) modified from Li et al. (2014) and Kang et al. (2020).
