Status, Gaps and Perspectives of Powdery Mildew Resistance Research and Breeding in Cucurbits

Figures & data

Table 1. Commonly produced Cucurbita fruit morphotypes (Paris et al., 2012b; Khoury et al., 2020; Grumet et al., 2021).

Species	Morphotypes
C. pepo subsp. pepo	Cocozelle, pumpkin, spaghetti squash, vegetable marrow, zucchini
C. pepo subsp. ovifera	Acorn, crookneck, delicata, scallop, straightneck
C. moschata	Butternut, cheese pumpkin, japonica, tropical (calabaza)
C. maxima	Banana, buttercup/kobocha, giant pumpkin, hubbard, kuri, turban
C. ficifolia	Figleaf gourd
C. argyrosperma subsp. argyrosperma	Cushaw

Table 2. Seven Citrullus species summarized from Renner et al. (2017), all are 2n = 22 except C. naudinianus (2n = 24).

Species	Common names and distinguishing characteristics
C. amarus Schrad.	Citron melon, annual, monoecious, cultivated, wild form in southern Africa
C. ecirrhosus Cogn.	Tendril-less melon, perennial, monoecious, endemic to southern Africa
C. mucosospermus (Fursa) Fursa	Egusi melon, annual, monoecious, cultivated, now distributed in western Africa
C. lanatus (Thunb.) Matsum. & Nakai	Watermelon, annual, monoecious, cultivated, including var. cordophanus (Ter-Avan.) Fursa
C. rehmii De Winter	Annual, monoecious, endemic to southern Africa
C. colocynthis (L.) Schrad.	Colocynth, perennial, monoecious, cultivated, widely distributed in northern Africa and southwestern and central Asia
C. naudinianus (Sond.) Hook.f.	Perennial, dioecious, sub-Saharan Africa

Figure 1. Macroscopic symptoms of cucurbit powdery mildew on leaves, stems, flower and fruit of eight representatives of Cucurbitaceae: (A) cucumber (Cucumis sativus); (B,C) melon (Cucumis melo); (D,E) summer squash (Cucurbita pepo); (F,G) winter squash (Cucurbita moschata); (H,I) watermelon (Citrullus lanatus); (J) bitter gourd (Momordica charantia); (K) bottle gourd (Lagenaria siceraria); (L) wax gourd (Benincasa hispida). Photo credits: B. Sedláková (A–D, F–I, K–L), N. Dhillon (E,J).

Figure 2. Microscopic characters of cucumber powdery mildews: (A) Golovinomyces orontii (conidia); (B) Podosphaera xanthii (conidia); (C) Leveillula taurica (primary conidia); (D) L. taurica (secondary conidia); (E) G. orontii (conidiophores); (F) P. xanthii (conidiophores); (G) L. taurica (conidiophores); (H) G. orontii (chasmothecium); (I) P. xanthii (chasmothecium); (J) L. taurica (chasmothecium). Photo credits: A. Lebeda (A,B), S. A. Khodaparast (C,D,G,J), L. Trecate (E,F), B. Sedláková (H,I). Bar represents: 10 µm (A–D), 20 µm (E–G), 50 µm (H,I) and 100 µm (J).

Table 3. Current and historical designations of seven Erysiphales species parasitizing members of the Cucurbitaceae family.

Species	References
Erysiphe actinostemmatis U. Braun, 1983^a	Braun (1983)
Neoerysiphe sechii Gregorio-Cipriano & D. González, 2020^a	Gregorio-Cipriano et al. (2020)
Leveillula taurica (Lév.) G. Arnaud, 1921	Arnaud (1921)
Oidiopsis taurica (Lév.) E.S. Salmon 1906	Salmon (1906)
Erysiphe taurica Lév., 1842^a	Demidov (1842)
Podosphaera xanthii (Castagne) U. Braun & Shishkoff, 2000	Braun and Takamatsu (2000)
Sphaerotheca xanthii (Castagne) L. Junell 1966	Junell (1966)
Sphaerotheca fuliginea f. cucurbitae Jacz. 1927	Jaczewski (1927)
Erysiphe xanthii Castagne 1845^a	Castagne (1845)
Golovinomyces orontii (Castagne) Heluta, 1988	Heluta (1988)
Erysiphe cichoracearum s.l. Braun 1987	De Candolle (1805) Braun (1987)
Erysiphe polyphaga Hammarl. 1945	Hammarlund (1945)
Erysiphe orontii Castagne 1851^a	Castagne (1851)
Golovinomyces tabaci (Sawada) H.D. Shin, S. Takam. & L. Kiss, 2019	Braun et al. (2019)
Golovinomyces cucurbitacearum (R.Y. Zheng & G.Q. Chen) Vakal. & Kliron. 2001	Vakalounakis and Klironomou (2001)
Erysiphe cucurbitacearum R.Y. Zheng & G.Q. Chen 1981	Zheng and Chen (1981)
Erysiphe tabaci Sawada 1928^a	Sawada (1928)
Golovinomyces bolayi S.Takam., Lebeda & M. Götz, 2019^a	Braun et al. (2019)

^a Basionym per www.mycobank.org.

Table 4. GRIN^a accession numbers, septet numbers, sources and origins of the ICPMI^b melon (Cucumis melo) cucurbit powdery mildew race differentials (Lebeda et al., 2016a; 2016b; 2018a; 2018b; 2021a; 2021b).

		Race differential
GRIN no.	Septet	Primary name	Other name(s)	Source^c	Origin
ICPMI 1 01	1.1	Iran H	–	INRA	Iran
ICPMI 1 02	1.2	Védrantais	M 319^d	INRA	France
ICPMI 1 03	1.3	PI 179901	Teti	USDA	India
ICPMI 1 04	1.4	PI 234607	Sweet Melon	USDA	South Africa
ICPMI 1 05	1.5	AR HBJ	AR Hale’s Best Jumbo	USDA	USA
ICPMI 1 06	1.6	PMR 45	M 321^d	USDA	USA
ICPMI 1 07	1.7	PMR 6	Ames 26810	USDA	USA
ICPMI 1 08	2.1	WMR 29	M 322^d	USDA	USA
ICPMI 1 09	2.2	Edisto 47	NSL 34600	Clemson Univ.	USA
ICPMI 1 10	2.3	PI 414723	LJ 90234	USDA	India
ICPMI 1 11	2.4	PMR 5	Ames 26809	USDA	USA
ICPMI 1 12	2.5	PI 124112	Koelz 2564	USDA	India
ICPMI 1 13	2.6	MR-1	Ames 8578	USDA	USA
ICPMI 1 14	2.7	PI 124111	Koelz 2563	USDA	India
ICPMI 1 15	3.1	PI 313970	PI 315410 VIR 5682 LJ 90625	USDA	India
ICPMI 1 16	3.2	Noy Yizréel	–	Bar Ilan Univ.	Israel
ICPMI 1 17	3.3	PI 236355	–	USDA	England
ICPMI 1 18	3.4	Negro	–	Univ. Zaragoza	Spain
ICPMI 1 19	3.5	Amarillo	–	Univ. Zaragoza	Spain
ICPMI 1 20	3.6	Nantais Oblong	M 320^d	INRA	France
ICPMI 1 21	3.7	Ames 31282	=	USDA	China
ICPMI 1 22	4.1	SVI105	=	INRA	France

^a GRIN (Germplasm Resources Information Network), seeds of the differential set are available upon request: https://npgsweb.ars-grin.gov/gringlobal/search. ^bICPMI (International Cucurbit Powdery Mildew Intiative). cINRA = L'Institut National de la Recherche Agronomique, Montfavet (France); USDA = United States Department of Agriculture, Agricultural Research Service. ^dDesignation by M. Pitrat, INRA, Montfavet (France) of seed provided to A. Lebeda in 1997.

Table 5. Cucumber (Cucumis sativus) genes (synonyms) controlling responses to Podosphaera xanthii and Golovinomyces orontii, and their respective sources per Wehner (2005-2006) and Weng and Wehner (2016).

Gene^a	Source	Race	Remark	Reference
P. xanthii
pm-1	Natuhusinari or Natsufushinari	Not specified		Hujieda and Akiya (1962), Kooistra (1971), Shanmugasundaram et al. (1972)
pm-2	Natuhusinari or Natsufushinari	Not specified		Fujieda and Akiya (1962), Kooistra (1971), Shanmugasundaram et al. (1972)
pm-3	PI 200815, PI 200818	Not specified		Kooistra (1971), Shanmugasundaram et al. (1972)
pm-h (s, pm)	Gy 2 cp cp, Spartan Salad, Wis. 2757	Not specified	Resistance noted as no fungal symptoms appearing on seedling cotyledon, recessive to susceptibility (Pm-h from “SMR 18”)	Fanourakis (1984), Shanmugasundaram et al. (1971b)
pm5.1 (CsMLO-1, CsMLO8,pm-h)	isolated from leaves of cucumber grown in a greenhouse	Not specified	Major mlo-type QTL, pm5.1, that seems to co-localize with pm-h	Nie et al. (2015a; 2015b)
pm-h (s, pm)		Hypocotyl resistance	Quantitative; pm-h played a major role in whole plant PM resistance; located in chromosome 5; may be the same as pm5.1.	Shanmugasundaram et al. (1971a; 1971b); de Ruiter et al. (2008); He et al. (2013)
PM species not specified
Pm1.1	North China type cucumber line Jin5-508	Not specified	Dominant major- QTL located in a 41.1 kb region of chromosome 1 harboring two tandemly arrayed cysteine rich receptor-like protein kinase genes	Xu et al. (2016b)

Table 6. Sources of resistance, mapped and cloned genes/quantitative trait loci (QTL) for powdery mildew resistance in cucumber (Cucumis sativus) summarized from Liu et al. (2021).

Source	Mapping population	Gene/QTL	Chromosome	Causal Gene	Reference
Puerto Rico 37	–	–	–	–	Smith (1948)
PI 197087	–	–	–	–	Barnes and Epps (1956)
Yomaki	–	–	–	–	Wilson et al. (1956)
Natsufushinari	–	–	–	–	Kooistra (1968)
PI 197088-1	PI 197088-1 × Santou RIL	–	1, 5, 6, 7		Sakata et al. (2006)
594	F6: 7S94 × S06 RIL	pm1.1, pm2.1, pm4.1, pm6.1	1, 2, 4, 6		Liu et al.(2008)
WIS2757	F2 WIS2757 × 19032	–	5		Zhang et al. (2008)
K8	F2 and F2: 3 K8 × K18	pm5.1, pm5.2, pm5.3, pm6.1	5, 6		Zhang et al. (2011a)
WI 2757 CS-PMR1	F2: 3 WI2757 × True Lemon CS.PMR1 (derived from PI	pm1.1, pm1.2, pm3.1, pm4.1, pm5.1, pm5.2	1, 3, 4, 5		He et al.(2013)
	197088 × Santou) RIL	9 QTL	All except 7		Fukino et al. (2013)
S1003	S1003 × S1001 BC3F1 and BC2F2	pm5.1	5	CSaMLO8 (CSMLO1)	Nie et al. (2015a, 2015b)
Jin5-508	Jin5-508 × D8 F2 and RIL	pm1.1	1		Xu et al. (2016b)
NCG122	F2 NCG122 × NCG121	pm-s	5		Liu et al. (2017)
PI 197088	PI 197088 × Coolgreen RIL	pm1.1, pm2.1, pm5.1, pm6.1	1, 2, 5, 6		Wang et al. (2018)
IL52	IL52 × Changchunmici RIL	pm	5	Csa5M622830	Zhang et al. (2018b)
PM-R	F2 PM-R × PM-S	pm5.2, pm6.1	5, 6	CsGy5G015660	Zhang et al. (2021a, 2021b)

Table 7. Melon (Cucumis melo) resistance genes and quantitative trait loci (QTL) to Golovinomyces orontii (Go) and Podosphaera xanthii (Px) and their sources as summarized by Dogimont and Sari (2022).

Gene symbol		Character	Linkage group^a	Reference
Preferred	Synonym
Golovinomyces orontii (Go)
Pm-E	–	Powdery mildew resistance-E. Interacts with Pm-C in PMR 5.		Epinat et al. (1993)
Pm-F	–	Powdery mildew resistance-F. Interacts with Pm-G in PI 124112.		Epinat et al. (1993)
Pm-G	–	Powdery mildew resistance-G. Interacts with Pm-F in PI 124112.		Epinat et al. (1993)
Pm-H	–	Powdery mildew resistance-H. Resistance to Go in Nantais Oblong.		Epinat et al. (1993)
Golovinomyces orontii (Go) and Podosphaera xanthii (Px)
PmXII.1	–	Powdery mildew resistance XII.I. Resistance to Px races 1, 2 and 5 and Go race 1 in PI 124112.	XII	Perchepied et al. (2005)
Podosphaera xanthii (Px)
Pm-1	Pm^1	Powdery mildew resistance-2. Interacts with Pm-1; Resistance to race 1 in PMR 5 with Pm-1.		Jagger et al. (1938b)
Pm-2	Pm^2 Pm-C ?	Powdery mildew resistance-2. Interacts with Pm-1; Resistance to race 2 in PMR 5 with Pm-1.		Bohn and Whitaker (1964)
Pm-3	Pm^3	Powdery mildew resistance-3. Resistance to race 1 in PI 124111.	7	Harwood and Markarian (1968a, 1968b)
Pm-4	Pm^4	Powdery mildew resistance-4. Resistance to race 1 in PI 124112.		Harwood and Markarian (1968a, 1968b)
Pm-5	Pm^5	Powdery mildew resistance-5. Resistance to race 1 in PI 124112.		Harwood and Markarian (1968a, 1968b)
Pm-6	–	Powdery mildew resistance-6. Resistance to race 2 in PI 124111.		Kenigsbuch and Cohen (1989)
Pm-7	–	Powdery mildew resistance-7. Resistance to race 1 in PI 414723.		Anagnostou et al. (2000)
Pm-8	–	Powdery mildew resistance-8. Resistance to race pxCh1 in Ames 31282 (formerly PI 134198)		Liu et al. (2010)
Pm- R	-	Powdery mildew resistance-R. Resistance to races 1, 2, and 5 in TGR-1551.	V	Yuste-Lisbona et al. (2011a)
pm-S	–	powdery mildew resistance-S. Resistance to race S in PI 313970.		McCreight and Coffey (2011)
Pm-w	Pm-B?	Powdery mildew resistance-w. Resistance to race 2 in WMR 29.	2, V	Pitrat (1991)
Pm- x	–	Powdery mildew resistance-x. Resistance to in PI 414723.	4, II	Pitrat (1991)
Pm-y	–	Powdery mildew resistance-y. Resistance to Px in VA 435	7, XII	Pitrat (1991)
pm-z1	Pm-z	Powdery mildew resistance-z. Resistance of true leaves to race 1 in PI 313970.		McCreight (2003)
Pm-z2US	Pm-z	Powdery mildew resistance-z2US. Semi-dominant resistance of true leaves to race 2US in PI 313970.		McCreight (2003)
pm-zC2US	Pm-z	Powdery mildew resistance-zC2US. Resistance of cotyledons to race 2US in PI 313970.		McCreight (2003)
PmV.1	–	Powdery mildew resistance V.1. Resistance to races 1, 2 and 3 in PI 124112.	V	Perchepied et al. (2005)
PMRI	–	Powdery mildew resistance RI. Resistance to race 2 of true leaves in MR-1. Epistatic to pmrs.	XII	Cui et al. (2022a)
pmrs	–	Powdery mildew resistance stem. Resistance to race 2 in stem of MR-1. Hypostatic to PMRI.	X	Cui et al. (2022a)
BPm12.1		BPm12.1 from MR-1 [58] QTL		Li et al. (2017)
Pm2.1		Powdery mildew 2.1. Resistance to race 2F in PMR 6.	II	Cui et al. (2020)
pm12.1		Powdery mildew 12.1. Resistance to race 2F in PMR 6.	XII	Cui et al. (2020)
Pm-x1,5		Powdery mildew x1,5. Resistance to races 1 and 5 in PI 414723.	II	Fazza et al. (2013)
Pm-x3		Powdery mildew 3. Resistance to race 3 in PI 414723.	II	Fazza et al. (2013)
Pm-AN		Powdery mildew An02. Resistance to race 1 in Ano2.	V	Wang et al. (2011)
Pmr2F		Powdery mildew race-2F. Resistance to race 2F in PI 124111		Zhang et al. (2023a)
Pm-Edisto47-1		Powdery mildew Edisto47-1. Resistance to race 1 in Edisto 47. Two dominant genes.	II	Ning et al. (2014)

^a Arabic numbers per Pitrat (1991) and Roman numerals per Périn et al. (2002) correspond to chromosome numbers per Garcia-Mas et al. (2012). QTL indicated with boldface.

Table 8. Melon (Cucumis melo) quantitative trait loci (QTL) for resistance to Podosphaera xanthii, including description and number of reported QTL, and their respective parental lines (Dogimont and Sari, 2022).

QTL description and parents	References
Two major QTL in Védrantais × PI 124112, PmV.1 in the linkage group V for races 1, 2, and 3 and PmXII.1 in the linkage group XII for resistance to races 1, 2 and 5 and to Golovinomyces cichoracearum race 1.	Perchepied et al. (2005)
Two QTL in TGR-1551 × Bola de Ora, a major one, dominant (LG V) and a minor one, recessive (LG VIII).	Yuste-Lisbona et al. (2010b, 2011a)
Two linked loci in linkage group II, one for resistance to races 1 and 5 (denominated Pm-x1,5), the second to race 3 (denominated Pm-x3), located 5.1 cM apart in PI 414723 × Vedrantais.	Fazza et al. (2013)
Major QTL BPm12.1 on chr. 12, in MR-1 × Top Mark.	Li et al. (2017)
Resistance to Px1A in Edisto 47 controlled by two dominant genes mapped on LGII and LGV and resistance to Px1B controlled by one dominant gene (Pm-Edisto47-1) in Edisto 47 × Queen.	Ning et al. (2014)
Resistance in MR-1 leaves linked to dominant gene PMRl on chr. 12, whereas stem resistance was under the control of a recessive gene (pmrs) on chr. 10, with the dominant gene epistatic to the recessive gene.	Cui et al. (2022a)

Table 9. Cucurbita spp. genes for cucurbit powdery mildew (CPM) resistance (Paris and Brown, 2005; Paris and Kabelka, 2009; Paris and Padley, 2014-2015).

Symbol	Source	CPM species^a	Remark	Reference
Pm	C. lundelliana	Gc	Powdery mildew resistance	Rhodes (1964)
Pm-0	C. okeechobeensis C. pepo	Px	Powdery mildew resistance-0; transferred from C. okeechobeensis to C. pepo; not known if this is the same or different locus from Pm	Contin (1978); Jahn et al. (2002); Cohen et al. (2003)
pm-1	C. moschata	Gc	Powdery mildew resistance-1; series of three alleles: pm-1^P for high susceptibility from Ponca dominant to pm-1^L for resistance from La Primera, which is dominant to pm-1^W for susceptibility in Waltham Butternut	Adeniji and Coyne (1983)
pm-2	C. moschata	Gc	Powdery mildew resistance-2; allele pm-2^S for resistance in Seminole is recessive to Pm-2 for susceptibility in Ponca	Adeniji and Coyne (1983)

^aGc: Golovinomyces cichoracearum; Px: Podosphaera xanthii.

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