Comparative association mapping reveals conservation of major gene resistance to white pine blister rust in southwestern white pine (Pinus strobiformis) and limber pine (P. flexilis)

All native North American white pines are highly susceptible to white pine blister rust (WPBR) caused by Cronartium ribicola. Understanding genomic diversity and molecular mechanisms underlying genetic resistance to WPBR remains one of the great challenges in improvement of white pines. To compare major gene resistance (MGR) present in two species, southwestern white pine (Pinus strobiformis) Cr3 and limber pine (P. flexilis) Cr4, we performed association analyses of Cr3-controlled resistant traits using SNP assays designed with Cr4-linked polymorphic genes. We found that ~ 70% of P. flexilis SNPs were transferable to P. strobiformis. Furthermore, several Cr4-linked SNPs were significantly associated with the Cr3-controlled traits in P. strobiformis families. The most significantly associated SNP (M326511_1126R) almost co-localized with Cr4 on the Pinus consensus linkage group 8 (LG-8), suggesting that Cr3 and Cr4 might be the same R locus, or have localizations very close to each other in the syntenic region of the P. strobiformis and P. flexilis genomes. M326511_1126R was identified as a non-synonymous SNP, causing amino acid change (Val376Ile) in a putative pectin acetylesterase (PAE), with coding sequences identical between the two species. Moreover, top Cr3-associated SNPs were further developed as TaqMan genotyping assays, suggesting their usefulness as marker-assisted selection (MAS) tools to distinguish genotypes between quantitative resistance (QR) and MGR. This work demonstrates the successful transferability of SNP markers between two closely related white pine species in the hybrid zone, and the possibility for deployment of MAS tools to facilitate long-term WPBR management in P. strobiformis breeding and conservation.

Download Full-text

Genetic resistance to white pine blister rust in limber pine (Pinus flexilis): major gene resistance in a northern population

Canadian Journal of Forest Research ◽

10.1139/cjfr-2016-0128 ◽

2016 ◽

Vol 46 (9) ◽

pp. 1173-1178 ◽

Cited By ~ 6

Author(s):

Richard A. Sniezko ◽

Robert Danchok ◽

Douglas P. Savin ◽

Jun-Jun Liu ◽

Angelia Kegley

Keyword(s):

Major Gene ◽

Genetic Resistance ◽

The United States ◽

White Pine Blister Rust ◽

White Pine ◽

Pinus Flexilis ◽

Limber Pine ◽

Blister Rust ◽

Major Gene Resistance ◽

The Status

Limber pine, Pinus flexilis E. James, a wide-ranging tree species in western North America, is highly susceptible to white pine blister rust (WPBR), caused by the non-native fungal pathogen Cronartium ribicola J.C. Fisch. The Canadian populations in particular have been heavily impacted, and in 2014, limber pine was designated endangered in Canada by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC). Little is known about genetic resistance to WPBR in limber pine, but major gene resistance (MGR) has been characterized in some populations in the United States. This study examines resistance in seedling families from 13 parent trees from British Columbia, Alberta, and Oregon, representing the northern- and northwestern-most populations. Most families were susceptible, with 100% of the seedlings cankered, but one family from Alberta segregated 1:1 for cankered and canker free. This is the first report of (a) MGR in Canada of any of the four species of five-needle pines native to Canada and (b) any resistance in limber pine in Canadian populations and is the northernmost known incidence of putative R-gene resistance in a natural stand of any five-needle pine species. Many of the Canadian selections were from stands with high incidence of WPBR infection, and their high susceptibility in this trial suggests that further infection and mortality is likely in the Canadian populations.

Download Full-text

White Pine Blister Rust Resistance in Limber Pine: Evidence for a Major Gene

Phytopathology ◽

10.1094/phyto-04-13-0092-r ◽

2014 ◽

Vol 104 (2) ◽

pp. 163-173 ◽

Cited By ~ 25

Author(s):

A. W. Schoettle ◽

R. A. Sniezko ◽

A. Kegley ◽

K. S. Burns

Keyword(s):

Major Gene ◽

Management Strategies ◽

Genetic Resistance ◽

Stress Factors ◽

R Gene ◽

White Pine Blister Rust ◽

White Pine ◽

Individual Tree ◽

Limber Pine ◽

Blister Rust

Limber pine (Pinus flexilis) is being threatened by the lethal disease white pine blister rust caused by the non-native pathogen Cronartium ribicola. The types and frequencies of genetic resistance to the rust will likely determine the potential success of restoration or proactive measures. These first extensive inoculation trials using individual tree seed collections from >100 limber pine trees confirm that genetic segregation of a stem symptom-free trait to blister rust is consistent with inheritance by a single dominant resistance (R) gene, and the resistance allele appears to be distinct from the R allele in western white pine. Following previous conventions, we are naming the R gene for limber pine “Cr4.” The frequency of the Cr4 allele across healthy and recently invaded populations in the Southern Rocky Mountains was unexpectedly high (5.0%, ranging from 0 to 13.9%). Cr4 is in equilibrium, suggesting that it is not a product of a recent mutation and may have other adaptive significance within the species, possibly related to other abiotic or biotic stress factors. The identification of Cr4 in native populations of limber pine early in the invasion progress in this region provides useful information for predicting near-term impacts and structuring long-term management strategies.

Download Full-text

Evidence of Cytoplasmic Inheritance of Virulence in Cronartium ribicola to Major Gene Resistance in Sugar Pine

Phytopathology ◽

10.1094/phyto.1999.89.3.192 ◽

1999 ◽

Vol 89 (3) ◽

pp. 192-196 ◽

Cited By ~ 9

Author(s):

Bohun B. Kinloch ◽

Gayle E. Dupper

Keyword(s):

Infection Type ◽

Major Gene ◽

Nuclear Gene ◽

Cronartium Ribicola ◽

White Pine Blister Rust ◽

White Pine ◽

Mendelian Segregation ◽

Blister Rust ◽

Major Gene Resistance ◽

Sugar Pine

Tests for Mendelian segregation of virulence and avirulence in Cronartium ribicola, causal agent of white pine blister rust, to a major gene (R) for resistance in sugar pine were made using haploid basidiospore progenies from single diploid telia as inoculum on resistant genotypes. The telia were sampled from a small deme in the Siskyou Mountains of northern California, where a few mature sugar pines known to be Rr genotypes had become infected after withstanding the chronic blister rust epidemic for several decades and where intermediate frequencies of virulence in the ambient basidiospore population were subsequently measured. Infection type on inoculated seedlings with R was qualitative: all progenies of 81 single telia tested over 3 different years were either virulent (compatible) or avirulent (inducing hypersensitive necrosis), never a mixture of both reactions. The complete absence of heterozygotes in the telia population is strong evidence that virulence is not controlled by a nuclear gene. The data are consistent with earlier tests showing that basidiospore inoculum derived from aeciospores isolated from infected Rr trees produced mostly (>90%) virulent reactions on R— seedlings. The evidence indicates that transmission of virulence is uniparental via the cytoplasm of aeciospores. Exchange of spermatia between haploid thalli does not appear to be involved.

Download Full-text

Influence of Host Resistance on the Genetic Structure of the White Pine Blister Rust Fungus in the Western United States

Phytopathology ◽

10.1094/phyto-98-4-0413 ◽

2008 ◽

Vol 98 (4) ◽

pp. 413-420 ◽

Cited By ~ 12

Author(s):

B. A. Richardson ◽

N. B. Klopfenstein ◽

P. J. Zambino ◽

G. I. McDonald ◽

B. W. Geils ◽

...

Keyword(s):

United States ◽

Genetic Structure ◽

North America ◽

Major Gene ◽

Western United States ◽

White Pine Blister Rust ◽

White Pine ◽

Blister Rust ◽

Major Gene Resistance ◽

Sugar Pine

Cronartium ribicola, the causal agent of white pine blister rust, has been devastating to five-needled white pines in North America since its introduction nearly a century ago. However, dynamic and complex interactions occur among C. ribicola, five-needled white pines, and the environment. To examine potential evolutionary influences on genetic structure and diversity of C. ribicola in western United States, population genetic analyses of C. ribicola were conducted using amplified fragment length polymorphism (AFLP) molecular markers. The fungus was sampled at six sites. Collections for two of the six sites were from separate plantings of resistant-selected western white pine and sugar pine. Heterozygosity based on polymorphic loci among populations ranged from 0.28 to 0.40, with resistant-selected plantations at the extremes. Genetic differentiation was also highest between these two populations. Principal coordinates analysis and Bayesian assignment placed most isolates that are putative carriers of virulence to major-gene resistance into a discernable cluster, while other isolates showed no clustering by site or host species. These results indicate that C. ribicola in western North America is not genetically uniform, despite its presumed single site of introduction and relatively brief residence. Moreover, major-gene resistance appears to have imposed strong selection on the rust, resulting in reduced genetic diversity. In contrast, no evidence of selection was observed in C. ribicola from hosts that exhibit only multigenic resistance.

Download Full-text

Cotyledon test for major gene resistance to white pine blister rust in sugar pine

Canadian Journal of Botany ◽

10.1139/b80-221 ◽

1980 ◽

Vol 58 (17) ◽

pp. 1912-1914 ◽

Cited By ~ 14

Author(s):

Bohun B. Kinloch Jr. ◽

Mardi Comstock

Keyword(s):

Major Gene ◽

White Pine Blister Rust ◽

White Pine ◽

Blister Rust ◽

Pine Seedlings ◽

Major Gene Resistance ◽

Sugar Pine ◽

Time Required ◽

Resistant Genotypes

Major gene resistance (hypersensitivity) to white pine blister rust can be detected on cotyledons of inoculated sugar pine seedlings shortly after germination. The cotyledon test reduces the time required for evaluating resistant genotypes from a few years to a few weeks.

Download Full-text

Risk of white pine blister rust to limber pine in Colorado and Wyoming, USA

Forest Pathology ◽

10.1111/efp.12065 ◽

2013 ◽

Vol 44 (1) ◽

pp. 21-38 ◽

Cited By ~ 10

Author(s):

H. S. J. Kearns ◽

W. R. Jacobi ◽

R. M. Reich ◽

R. L. Flynn ◽

K. S. Burns ◽

...

Keyword(s):

White Pine Blister Rust ◽

White Pine ◽

Limber Pine ◽

Blister Rust

Download Full-text

Genetic mapping of Pinus flexilis major gene (Cr4) for resistance to white pine blister rust using transcriptome-based SNP genotyping

BMC Genomics ◽

10.1186/s12864-016-3079-2 ◽

2016 ◽

Vol 17 (1) ◽

Cited By ~ 16

Author(s):

Jun-Jun Liu ◽

Anna W. Schoettle ◽

Richard A. Sniezko ◽

Rona N. Sturrock ◽

Arezoo Zamany ◽

...

Keyword(s):

Genetic Mapping ◽

Major Gene ◽

Snp Genotyping ◽

White Pine Blister Rust ◽

White Pine ◽

Pinus Flexilis ◽

Blister Rust

Download Full-text

Changes in white pine blister rust infection and mortality in limber pine over time

Canadian Journal of Forest Research ◽

10.1139/cjfr-2013-0072 ◽

2013 ◽

Vol 43 (10) ◽

pp. 919-928 ◽

Cited By ~ 11

Author(s):

Cyndi M. Smith ◽

David W. Langor ◽

Colin Myrholm ◽

Jim Weber ◽

Cameron Gillies ◽

...

Keyword(s):

Mountain Pine Beetle ◽

Fire Suppression ◽

Basal Area ◽

White Pine Blister Rust ◽

White Pine ◽

Pinus Flexilis ◽

Limber Pine ◽

Blister Rust ◽

Dead Trees ◽

Pine Beetle

Limber pine (Pinus flexilis E. James) is under threat from white pine blister rust (WPBR), mountain pine beetle, drought, and fire suppression across its range in western North America. In 2003–2004, we established 85 plots to assess the mortality and incidence of WPBR on limber pine, and remeasured them in 2009. Infection was evident in 74% of the plots in 2003–2004 and 88% of the plots in 2009. The proportion of dead trees increased from 32% in 2003–2004 to 35% in 2009. The percentage of live trees infected increased from 33% in 2003–2004 to 43% in 2009. Mean live limber pine basal area in 2009 ranged from 0.03 to 77.8 m2/ha per plot. Twenty (24%) of the plots had no seedlings in the first measurement, but only 15% in the second measurement. Seedling infection was low (8% in 2003–2004 and 4% in 2009). In 12 plots that were measured three times, mortality increased from 30% of all trees in 1996 to 50% in 2003, then decreased to 46% in 2009. Infection decreased from 73% of live trees in 1996 to 46% in 2003, then increased to 66% in 2009. High mortality and infection levels suggest that the long-term persistence of many limber pine populations in the southern part of the study area are in jeopardy, and continued monitoring is needed to assist with management decisions.

Download Full-text

First Report of White Pine Blister Rust in Colorado

Plant Disease ◽

10.1094/pdis.2000.84.5.595d ◽

2000 ◽

Vol 84 (5) ◽

pp. 595-595 ◽

Cited By ~ 18

Author(s):

D. W. Johnson ◽

W. R. Jacobi

Keyword(s):

White Pine Blister Rust ◽

White Pine ◽

Pinus Flexilis ◽

Limber Pine ◽

Blister Rust ◽

Continental Divide ◽

Northern Colorado ◽

Fort Collins ◽

Park Road ◽

Ribes Spp

In June 1999, a survey was conducted north and west of Redfeather Lakes, CO (≈64 km northwest of Fort Collins) to determine the extent of white pine blister rust, caused by Cronartium ribicola. To date the disease has not been reported in Colorado on any of the known hosts. The survey was initiated after the disease was reported on limber pine, Pinus flexilis, in 1998. A total of 65 sections were traveled by driving passable roads within three townships in Larimer County in northern Colorado. Infected limber pines were observed in nine sections. Incidence of infected trees ranged from 3 to 50% of trees sampled. A minimum of 10 trees was sampled at each location. Where trees were more abundant, 40 trees were sampled. The highest incidence of blister rust was observed near the Colorado and Wyoming state line along Cherokee Park Road. Both main stem and branch cankers were observed. Cankers appeared to be 3 to 5 years old. Mortality of entire trees was not observed. Ribes spp. were observed in the vicinity of infected limber pines. However, no infection was noted on these alternate rust hosts. Infected trees were observed 18 km south of the Colorado and Wyoming state line. The southward spread of the disease into northern Colorado from infection sites in Wyoming appears to have proceeded slowly since reports of the disease in southern Wyoming during the 1970s (1). Blister rust has the potential to spread throughout the range of white pines in Colorado, which includes scattered populations of both limber and bristlecone pines, P. aristata, located along the Continental Divide from Wyoming to the Colorado and New Mexico state line. References: (1) D. B. Brown. Plant Dis. Rep. 62:905, 1978.

Download Full-text