Elite Upland Cotton Germplasm-Pool Assessment of Fusarium Wilt ...

Published September 6, 2013 Agronomy, Soils & Environmental Quality

Elite Upland Cotton Germplasm-Pool Assessment of Fusarium Wilt Resistance in California Robert B. Hutmacher, Mauricio Ulloa,* Steven D. Wright, B. Todd Campbell, Richard Percy, Ted Wallace, Gerald Myers, Fred Bourland, David Weaver, Peng Chee, Peggy Thaxton, Jinfa Zhang, Wayne Smith, Jane Dever, Vasu Kuraparthy, Daryl Bowman, Don Jones, and John Burke Abstract

During the past 9 yr, a new race of Fusarium (Fusarium oxysporum f. sp. vasinfectum [FOV Race 4]) has increasingly impacted cotton (Gossypium spp.) in the San Joaquin Valley of California. To assess the vulnerability of upland cotton (G. hirsutum L.) in California to FOV disease, elite upland germplasm lines from 13 U.S. public breeding programs across the Cotton Belt and commercial cultivars were evaluated for disease resistance to FOV Races 1 and 4. Ten independent replicated field trials were conducted: three in 2008, four in 2010, and three in 2011. Significant differences (P £ 0.05) were observed for disease severity index of leaves, vascular root staining, and plant survival values among the elite germplasm lines in all 3 yr for the levels of resistance–response to FOV Races 1 and 4. Also, significant interactions among germplasm lines, FOV races (1 and 4), and evaluation sites indicated that germplasm lines differed in mechanisms of plant-defense response for the two FOV races. Selected lines from programs in the states of Alabama, Arkansas, Louisiana, and Mississippi showed at least a moderate level of tolerance to both FOV races; however, several of these lines produced weak and coarse fibers. Based on these evaluations, many of the entries in public breeders’ current elite upland germplasm pools may be more susceptible than expected to some FOV races, and sources of acceptable levels of resistance may be limited when tested under infestation levels that resulted in only 5 to 35% plant survival in susceptible check cultivars.

C

otton is an economically important crop and provides the world’s leading natural fiber for the textile industry (Smith et al., 1999; Ulloa et al., 2007). The future of cotton improvement depends on plant characteristics conferring not only improved water-use efficiency and heat tolerance but also disease resistance. Integrating disease resistance into high-yielding, high-fiber-quality cultivars is one of the most important objectives in cotton breeding programs (Smith et al., R.B. Hutmacher, Dep. of Plant Science, Univ. of California-Davis, West Side Research and Extension Center, Five Points, CA 93624; M. Ulloa and J. Burke, USDA-ARS, Cropping Systems Research Lab., Plant Stress and Germplasm Development Unit, Lubbock, TX 79415; S.D. Wright, Univ. of California, Tulare, CA 93274; B.T. Campbell, USDA-ARS, Coastal Plains Soil and Water Conservation Research Center, Florence, SC 29501; R. Percy, USDA-ARS, Southern Plains Agricultural Research Center, Crop Germplasm Unit, College Station, TX 77845; T. Wallace, Mississippi State Univ., MS 39762; G. Myers, Agriculture Center, Louisiana State Univ., Baton Rouge, LA 70803; F. Bourland, Northeast Research and Extension Center, Univ. of Arkansas, Keiser, AR 72351; D. Weaver, Dep. of Agronomy and Soils, Auburn Univ., Auburn, AL 36849; P. Chee, Univ. of Georgia, National Environmentally Sound Production Agriculture Laboratory, Tifton, GA 31793; P. Thaxton, Delta Research and Extension Center, Stoneville, MS 38776; J. Zhang, Dep. of Plant and Environmental Sciences, New Mexico State Univ., Las Cruces, NM 88003; W. Smith, Dep. Crop and Soil Sciences, Texas A&M Univ., College Station, TX 77843; J. Dever, Texas A&M AgriLife Research and Extension Center, Lubbock, TX 79403; V. Kuraparthy and D. Bowman, Dep. of Crop Science, North Carolina State Univ., Raleigh, NC 27695; and D. Jones, Cotton Incorporated, Cary, NC 27513. Received 3 June 2013. *Corresponding author ([email protected]). Published in Agron. J. 105:1635–1644 (2013) doi:10.2134/agronj2013.0264 Copyright © 2013 by the American Society of Agronomy, 5585 Guilford Road, Madison, WI 53711. All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.

1999; Ulloa et al., 2009). Host-plant resistance can be a highly effective and economical approach for dealing with disease threats such as FOV and limiting yield loss in cotton (Hutmacher et al., 2011; Ulloa et al., 2010, 2011, 2013). Eight genotypes of FOV, called races, have been described (Skovgaard et al., 2001; Kim et al., 2005). Before 1986, only Races 1 and 2 were known to occur on significant acreage in the United States (DeVay, 1986). Since FOV disease in cotton was first reported in California in 1959 (Garber and Paxman, 1963), FOV Races 1 or 2 were recognized as the causal organism and were typically found in sandy soils with root-knot nematode (RKN) [Meloidogyne incognita (Kofoid and White) Chitwood] (Garber et al., 1979; Veech, 1984; Bell, 1984). The FOV fungal pathogen is a soil inhabitant that can survive for long periods in the absence of a host. Consequently, it is nearly impossible to eradicate from a field. A marked increased in the susceptibility of cultivars to FOV Race 1 was noted in the presence of RKN (Garber et al., 1979). Cotton developed for resistance to FOV on soils infested with RKN usually maintained their resistance when simultaneously challenged by both organisms, FOV Race 1 and RKN (Sasser, 1972; Heald and Orr, 1982). In 2005, University of California-Davis scientists (Kim et al., 2005) identified additional FOV races (1, 3, 4, and 8) in California soils. During the past 9 yr, FOV Race 4 has increasingly impacted cotton fields in the San Joaquin Valley (SJV) of California (Hutmacher et al., 2011). In field soils with relatively high levels of FOV Race 4, extensive disease symptoms Abbreviations: DSI, disease severity index of leaves; FOV, Fusarium wilt; PS, plant survival; RBTN, Regional Breeders Testing Network; RKN, rootknot nematode; SJV, San Joaquin Valley; VRS, disease index of vascular root staining.

A g ro n o my J o u r n a l • Vo l u m e 10 5 , I s s u e 6 • 2 013

1635

and, in some cases, large reductions in plant survival were observed in clay loam and loam soils even when RKN populations and root damage from nematodes were nonexistent or extremely low. Major plant damage and losses with FOV Race 4 in the absence of RKN is in marked contrast to observations with FOV Race 1. Acala and non-Acala upland germplasm tested for susceptibility to FOV Race 4 were infected by FOV Race 4 at field sites or in greenhouse artificial inoculation trials, showing mild to severe symptoms (Hutmacher et al., 2011; Ulloa et al., 2006, 2010, 2013). The four FOV races identified in California cotton by University of California-Davis scientists (Kim et al., 2005) were originally classified on the basis of pathogenicity tests on different cotton species—G. hirsutum, G. barbadense L., and G. arboreum L. (Armstrong and Armstrong, 1958, 1960, 1978; Ibrahim, 1966)—and by their pathogenicity on alfalfa (Medicago sativa), soybean [Glycine max (L.) Merr.], and tobacco (Nicotiana tabacum L.) (Armstrong and Armstrong, 1978). Presently, these races are categorized according to a number of genetic markers. Based on sequence differences in the translational elongation factor (EF-1a), phosphate permase (PHO), and b-tubulin (BT) genes and intergenic spacer (IGS) regions with restriction enzyme digests, worldwide strains of FOV can be classified into five major lineages (Kim et al., 2005). Recently, analyses with partial sequences from the above genes of 61 FOV isolates across the United States (Holmes et al., 2009) revealed four additional FOV genotypes, and for the first time, Races 3 and 8 were reported outside of California. The majority of these novel genotypes were from the state of Arkansas and were pathogenic to at least one cotton cultivar used in the study (Holmes et al., 2009). For breeders, it is important to understand the genetic inheritance of FOV based on host-plant resistance (Ulloa et al., 2013). In early genetic analyses, FOV resistance was reported to be determined by one or two major genes with complete to incomplete dominance and possibly additional minor genes (Mohamed, 1963; Smith and Dick, 1960; Ulloa et al., 2006). In recent genetic studies (Wang et al., 2009; Ulloa et al., 2011; Becerra et al., 2012), resistance to Races 1, 7, and the Australian FOV races was reported to be inherited through gene interactions detected in more than one chromosome. In addition, a major dominant gene was identified that conferred resistance to FOV Race 4 in the Pima S-6 germplasm line. The Fov4 gene appears to be located near a genome region on chromosome 14 marked with a quantitative trait locus Fov41-C14 and made the biggest contribution to the FOV Race 4 resistance of the generated F2 progeny (Ulloa et al., 2013). Collectively, these studies (Wang et al., 2009; Ulloa et al., 2011, 2013; Becerra et al., 2012) suggest a different gene specificity of FOV resistance in cotton (Fov1 [Race 1], chromosome 16; Fov4 [Race 4], chromosome 14; FW R [Race 7], chromosome 17; and Australian race Fov [AUS], chromosomes 6, 22, and 25) (Ulloa et al., 2013). A key component to improving breeding lines and germplasm is the ability to test their improvements in an extensive network of sites. The Regional Breeders Testing Network (RBTN) is a multienvironment trial (MET) supported by Cotton Incorporated (www.cottonrbtn.com or www.cottoninc.com/fiber/ AgriculturalDisciplines/Variety-Improvement/RBTN/). University and USDA-ARS cotton geneticists and breeders conduct 1636

a cooperative MET across the major cotton growing regions of the United States. At these MET sites, elite upland germplasm lines are tested for yield and fiber quality performance, biotic and abiotic stresses such as nematodes, tarnished plant bug, heat, and FOV and Verticillium wilt (Verticillium dahlia Kleb) resistance. In 2008, 2010, and 2011, the USDA-ARS Shafter Cotton Research Station and the University of California were involved in FOV host-plant resistance trials, evaluating advanced breeding lines from the RBTN group. Observations reported in recent years (Holmes et al., 2009; Kim et al., 2005; Kochman et al., 2002; Ulloa et al., 2006; Wang et al., 2004) have confirmed that FOV is becoming a recurring and potentially expanding threat to cotton production. Recent analyses with partial sequences of marker genes of 61 FOV isolates across the United States revealed four additional new FOV genotypes. The majority of these novel genotypes were from Arkansas and were pathogenic to at least one tested cotton cultivar used in the study (Holmes et al., 2009; Davis and Nichols, personal communication, 2010). In addition, little is known about resistance in U.S. upland and wild species of cotton to these FOV races or how soil type, soil pH, natural antagonists, and interactions with other pathogens (e.g., Verticillium and reniform nematode [Rotylenchulus reniformis] Linford and Oliveira) could affect this pathogen. Their complete host range is not well understood. Based on our current knowledge of the ecological factors that favor the strains of FOV, cotton production in broad areas of the United States could be at risk. The objective of the research reported here was to assess the vulnerability of upland cotton in the SJV of California to FOV disease through a series of field trial evaluations conducted at field sites infested with FOV Race 1 and RKN, and at separate sites found to be infested with FOV Race 4, in both cases using elite upland germplasm lines from 13 U.S. public breeding programs across the Cotton Belt and commercial cultivars. Results from our studies can be utilized in further genetic evaluations to identify sources of host plant resistance useful to breeders and of potential economic value to growers. Long-term management of Fusarium wilt in cotton will be enhanced by the development of resistant cultivars. Materials and Methods Germplasm and Cultivars Elite upland germplasm lines from the RBTN representing 13 public breeding/genetics programs from 10 states and check cultivars were used in this study (Table 1). The elite upland germplasm lines from the RBTN were evaluated for resistance to FOV Race 1 in the presence of RKN, for FOV Race 4 resistance, and for yield potential and fiber quality in 2008, 2010, and 2011 (Table 2). Upland and Pima (G. barbadense) cotton cultivars from private seed companies were included as additional comparison genotypes (Tables 1 and 2). Cultivars DP 393 (Monsanto Co., PVP no. 200400266), Fiber Max (FM) 958, (Bayer CropScience Co., PVP no. 200100208), SureGrow (SG) 105 (SureGrow Co., PVP no. 9900190), and Phytogen 72 (Phytogen Seed Co., PVP no. 200100115) cultivars were used as checks for yield and fiber quality characteristics. Upland cultivar Shorty (Ulloa et al., 2013) was used as a susceptible check for both races (1 and 4). Pima S-7 (Turcotte et al., 1992), Pima 3-79 (GB 1585), and Phytogen 72 were used as resistant checks Agronomy Journal • Volume 105, Issue 6 • 2013

Table 1. Elite germplasm lines from the Regional Breeders Testing Network representing 13 public breeding/genetics programs from 10 U.S. states. U.S. state Alabama

Institution Auburn Univ.

Breeder Weaver

2008 AU-5491 AU-5367 AU-6103 AU-1107

2010 AU3202 AU6001 AU3111 AU6202

2011 AU3202 AU3111 AU3223 AU3095

Arkansas

Univ. of Arkansas

Bourland

Ark0012-03-08 Ark0015-06-11 Ark0002-03-02 Ark0001-01-03 Ark008-22-10

Ark 0219-15 Ark 0203-11 Ark 0222-12 Ark 0232-24

Ark 0305-07 Ark M222-07 Ark 0316-36 Ark 0309-31 Ark 0304-23

Georgia

Univ. of Georgia

Chee

GA2004230 GA2004089 GA2004303 GA2006128

GA 2004143 GA 2006106 GA 2006053 GA 2007095

GA 2004143 GA 2008083 GA 2008057

Louisiana

Louisiana State Univ.

Myers

LA05307029 LA05307061 LA05307083 LA05307094

LA06307025 LA07307111 LA07307122 LA07307106

LA06307025 LA07307106 LA00405034

Mississippi

USDA-ARS

Meredith

MD25ne MD25Y

MD25-26ne MD 25-87Y MD 25-27Y

Mississippi State Univ.

Wallace

Thaxton

North Carolina New Mexico

South Carolina

Texas United States

North Carolina State Univ.

Kuraparthy

New Mexico State Univ.

Zhang

USDA-ARS

Campbell

Texas A&M Univ.

Dever (seed provided) Smith

private seed company

USDA-ARS

0033-6

NC09AZ09 NC05AZ06

NC08AZ21

Acala 1517-99 NM 03012

NM W1218 NM 06N1166 NM 03012 NM 06N1104

NM08N1562 NM08N1564 NM08N1084 Acala 1517-08 Acala 1517-99

PD99041 PD04012 PD03025 PD03011

PX03201-66-1 PD05041 PD05035 PX03202-65-1

PD 05069 PD 05070 PD 06001

TAM B182-34

LBB-07-21-311 TAM 03WZ-37

Tamcot 73

DP 393 FM 958 SG 105 Phytogen 72 Phytogen 800

DP 393 FM 958 SG 105 Phytogen 72

DP 393 FM 958 SG 105 Phytogen 72

USDA-ARS

Pima S-7

Pima S-7 Pima 3-79

Ulloa

SJ-07P-FR01 SJ-07P-FR02 SJ-07P-FR03 SJ-07P-FR04

TM-1 Pima S-6 Upland Shorty 096 Nem

Pima S-7 Pima S-6 TM-1 SJ-10P10 SJ-10P13 SJ-10P17 SJ-10P19

obsolete cultivars Phytogen Co.

California

0149-17 ne 0147-22 ne 0020-31 ne 0028-16 ne 8921-2-2-14-13-11 04PST-250 04-PST-275 04PST-246

Agronomy Journal • Volume 105, Issue 6 • 2013

1637

Table 2. Summary of independent infested field site evaluations of Fusarium wilt (FOV) and root-knot nematode (RKN) infection response, along with yield potential and fiber quality characteristics of elite upland cotton germplasm lines from the Regional Breeders Testing Network (RBTN) representing 13 public breeding/genetics programs from 10 U.S. states. Test† SCA08_FOVR1 SCA10_FOVR1 SCA10_YnF SCA11_FOVR1 FCA08_FOVR4 KCA08_FOVR4 KCA10_FOVR4 WSCA10_YnF KCA11_FOVR4 WSCA11_YnF

Year

Location

Planting date

Soil type

Evaluation response

2008 2010 2010 2011 2008 2008 2010 2010 2011 2011

Shafter Shafter Shafter Shafter Fresno Co. Kern Co. Kern Co. West Side Kern Co. West Side

24 Apr. 2008 3 May 2010 4 May 10 27 Apr. 2011 5 May 2008 28 Apr. 2008 25 May 2010 5 May 2010 18 May 2010 23 Apr. 2011

sandy loam sandy loam loam sandy loam clay loam clay loam clay loam clay loam clay loam clay loam

Response to FOV Race 1 + RKN Response to FOV Race 1 + RKN Yield potential and fiber traits Response to FOV Race 1 + RKN Response to FOV Race 4 Response to FOV Race 4 Response to FOV Race 4 Yield potential and fiber traits Response to FOV Race 4 Yield potential and fiber traits

† SCA08-11_FOVR1, replicated field evaluation conducted on a field site infested with FOV Race 1 and RKN at the Shafter Cotton Research Station, Shafter CA, and SC10_YnF, yield potential and fiber quality traits evaluated during the same test; FCA08_FOVR4, replicated field evaluation conducted on an infested field with FOV Race 4 at a Fresno County site; KCA08_FOVR4, replicated field evaluation conducted on an infested field with FOV Race 4 at a Kern County site; WSCA10_YnF, replicated field yield potential and fiber quality traits evaluation conducted at the West Side Research and Extension Center, Five Points, CA.

for FOV Race 1 and as susceptible checks for FOV Race 4. The Pima S-6 (Ulloa et al., 2013; CV-81 NSL183011), SJ-07-FR01 through SJ-07-FR04 (Ulloa et al., 2009), SJ-10P10, SJ-10P13, SJ-10P17, and SJ-10P19 germplasm lines (Ulloa et al., unpublished data, 2010) and Phytogen 800 (Phytogen Seed Co., S. Patent no. 7332.657) were used as resistant checks for both FOV races (1 and 4). Fusarium Wilt Evaluations Ten independent replicated field evaluations were conducted: three in 2008, four in 2010, and three in 2011 (Table 2). Additional information about the different trials conducted using the RBTN germplasm is presented in Table 2. In 2008, 2010, and 2011, we conducted evaluations at a sandy loam soil field site infested with FOV Race 1 + RKN (Field SCA0811_FOVR1 in Table 2). Entries were grown in one-row plots, 5 by 1 m, in a randomized complete block design with three replications. Five plants were randomly chosen per plot to be used as subsamples to obtain estimates of disease severity indices of leaves (DSI) and vascular root staining (VRS) at 81 d (2008), 92 d (2010), and 87 d (2011) after planting (Table 2). The number of main stem nodes (excluding the cotyledonary node) and plant height (measured from the cotyledon node to the uppermost node) were measured on each plant. Plant survival (PS) in each plot was recorded at 81 d (2008, Field SCA08_FOVR1), 92 d (2010, Field SCA10_FOVR1), and 87 d (2011, Field SCA11_FOVR1) after planting. The PS (expressed as a percentage) was calculated by dividing the total number of surviving plants on each sample date by the initial plant count made 12 to 14 d after planting and multiplying by 100. Evaluations were also conducted at clay loam soil field sites infested with FOV Race 4 in Fresno (Field FCA08_FOVR4) and Kern (Field KCA08- 11_FOVR4) counties in 2008, 2010, and 2011 (Table 2). Plants at these sites consistently developed severe FOV Race 4 symptoms, and infection of plants were confirmed to be by Race 4. Entries were grown in one-row plots, 5 by 1 m, in a randomized complete block or incomplete complete block design with three replications. The DSI, VRS, number of nodes, plant height, and PS were determined at 91 d (2008, Fresno County, Field FCA08_FOVR4), 92 d (2008, Kern County, Field KCA08_FOVR4), 48 d (2010, 1638

Kern County, Field KCA10_FOVR4), and 68 d (2011, Kern County, Field KFCA11_FOVR4) after planting (Table 2). Individual plants were rated for DSI based on the following scale: 0 = no symptoms, 1 = epinasty and slight dwarfing, 2 = 1 to 30% of leaves chlorotic, 3 = 31 to 80% of leaves chlorotic and severe stunting, 4 = 81 to 100% of leaves chlorotic, and 5 = plant death. Stems and the upper part of the primary root of the same plants were cut longitudinally and evaluated for VRS. The following scale was used for VRS: 0 = no vascular root staining evident, 1 = light vascular root staining evident as spotty areas, 2 = root staining more continuous, but lightcolored staining covering an area between one quarter and one half of the stem cross-section, 3 = moderate brown to black staining evident in a band encircling most of the stem crosssection, 4 = brown to black staining evident across most vascular tissue in stem cross-section, and 5 = plant severely damaged or plant dead, with staining evident throughout a cross-section of root tissue (Ulloa et al., 2013). To evaluate the performance of the elite germplasm lines of the RBTN group under SJV environments on non- FOVinfested fields and to compare them with check cultivars in 2010 and 2011, replicated field evaluations were conducted for yield potential and fiber quality characteristics at the Shafter Cotton Research Station, Shafter, CA (Field SCA10_YnF) and at the University of California West Side Research and Extension Center, Five Points, CA (Fields WSCA10_YnF and WSCA11_YnF) (Table 2). All tests were replicated four times in a randomized complete block design. Entries were planted in one-row plots varying from 9 to 14 by 1 m, depending on location. Fiber samples were obtained by hand picking 25-boll samples from each plot. All plots were machine harvested with a modified spindle picker to determine seed cotton yield. Fiber samples were subjected to high-volume instrument (HVI) fiber quality testing at Cotton Incorporated. The following agronomic data were included in the analysis of performance and comparisons of elite germplasm lines and check cultivars under SJV environments: seed cotton yield per plot (g), lint yield (kg/ha), and lint percentage (%). The following fiber quality characteristics were included: fiber length (upper half mean), fiber strength, fiber elongation, fineness (micronaire), and short fiber content (%). In addition, in 2011 from the WSCA11_YnF Agronomy Journal • Volume 105, Issue 6 • 2013

Fig. 1. Distribution of disease index of vascular root staining of Fusarium wilt (FOV) Races 1 and 4 (y axis scale from 0 to 5: 0 = no symptoms and 5 = plant dead) on check cultivars and elite germplasm lines from 10 public breeding/genetics programs from nine U.S. states: Arkansas, South Carolina, Georgia, Louisiana, Texas, Mississippi, Alabama, New Mexico, and California. Three independent replicated field evaluations were conducted in California in 2008: FOV Race 1 + root-knot nematode at Shafter Cotton Research Station, planted 24 Apr. 2008; FOV Race 4 at the Kern County site, planted 28 Apr. 2008; and FOV Race 4 at Fresno County site, planted 5 May 2008.

site, fiber samples were subjected to the advanced fiber information system (AFIS) instrument for analyzing fiber quality traits. Eight fiber traits were included: short fiber content (g/kg), number of nep size by weight (no./g), upper quartile of fiber length (mm), fiber span length (mm), seed coat fragment size (g), fiber fineness (millitex), immature fiber content by weight (g/kg), and maturity ratio (unit). Data Analyses Data were analyzed with PROC GLM (SAS version 9.2, SAS Institute) for different values of response (DSI, VRS, number of nodes, plant height, and PS) in 2008, 2010, and 2011. Mean separation among germplasm lines and check cultivars was conducted using the Waller–Duncan k-ratio procedure (Ott, 1988). In addition, genotype ´ sites and genotype ´ FOV race interactions were examined using PROC GLIMMIX and mean separations such as LSD and adjust = simulate (data not presented). Correlation analyses were performed to examine the similarity of response of the elite germplasm lines and check cultivars from the various evaluations of the different trials as indicated by FOV Races 1 and 4 plant infection using DSI, VRS, number of nodes, plant height, and PS. Similarity in plant response of the FOV Races 1 and 4 infection among germplasm lines and check cultivars was assessed by correlation analyses of VRS corresponding to each evaluation with DSI, VRS, number of nodes, plant height, and PS. All correlations were performed using PROC CORR in SAS (version 9.2, SAS Institute). Results Fusarium Wilt Resistance Evaluations Significant variation (P £ 0.05) in resistance response to FOV Races 1 and 4 was observed for the elite germplasm lines and check cultivars based on DSI and VRS values in the 2008, 2010, and 2011 evaluations. In 2008, at the SCA08_FOVR1 field site, VRS values of infection for FOV Race 1 + RKN on tolerant and resistant check cultivars such as upland Phytogen 72, Pima S-7, Phytogen 800, and the SJ-07P-FR01-04 lines

ranged from 0.27 to 1.27 (Fig. 1). At the SCA10_FOVR1 field site in 2010, VRS values on Phytogen 72, Pima S-6, and Pima S-7 ranged from 0.5 to 1.0. In 2011, similar responses for FOV Race 1 + RKN infection was observed on tolerant (VRS £ 2.0) and susceptible (VRS > 2.0) check cultivars at the Shafter Cotton Research Station field site (SCA11_FOVR1, data not presented). Significant variation (P £ 0.05) in plant height and PS was observed for the check cultivars when they were assessed for FOV Races 1 and 4 resistance (Fig. 2). Also at the SCA10_FOVR1 field site, PS at 92 d after planting for upland FOV Race 1 + RKN susceptible Shorty was 52.5%, while tolerant upland Phytogen 72 was 96.5% at the conclusion of the trial. The VRS and PS values were negatively correlated, ranging from r = –0.17 (2008) to r = –0.68 (2010) at P £ 0.05 within each race and evaluation site, indicating that a high VRS value for FOV Race 1 + RKN infection resulted in low PS. When we compared infested field evaluation sites (FOV Race 1 + RKN [Shafter site] and FOV Race 4 [Kern and Fresno counties]) (Table 2), significant differences (2008, P £ 0.05; 2010, P £ 0.06; 2011, P £ 0.05) were observed between FOV Race 1 + RKN and FOV Race 4 based on recorded VRS values for the elite germplasm and check cultivars. Overall, the results revealed interactions in disease response between assayed elite germplasm lines and check cultivars, FOV races (1 and 4), and evaluation sites (data not presented). For example, we observed that Pima S-7 and Acala Phytogen 72 responded differently to the two FOV races. Both entries were more susceptible to Race 4 at the FCA08_FOVR4 Fresno and KCA_FOVR4 Kern counties field sites than to FOV Race 1 + RKN at the SCA08_ FOVR1 Shafter field site (Fig. 1 and 2). At the SCA08_FOVR1 field site in 2008, the VRS and PS values of FOV Race 1 + RKN were 0.53 and 93.9%, respectively, for resistant check Pima S-7 and 0.27 and 78.7%, respectively, for resistant check Phytogen 72 (Fig. 1 and 2). In 2010, VRS and PS values were 1.0 and 88.6%, respectively, for Pima S-7 and 1.3 and 96.5%, respectively, for Phytogen 72 for FOV Race 1 + RKN.


1639

Fig. 2. Distribution of field plant survival (y axis scale from 0 to 100%) of check cultivars and elite germplasm lines from 10 public breeding/genetics programs from nine U.S. states: Arkansas, South Carolina, Georgia, Louisiana, Texas, Mississippi, Alabama, New Mexico, and California. Plant death was assumed to be due to disease infection of Fusarium wilt (FOV) Races 1 and 4. Three independent replicated field evaluations were conducted in California in 2008: FOV Race 1 + root-knot nematode at Shafter Cotton Research Station, planted 24 Apr. 2008; FOV Race 4 at the Kern County site, planted 28 Apr. 2008; and FOV Race 4 at Fresno County site, planted 5 May 2008.

Fig. 3. Distribution of disease index of vascular root staining of Fusarium wilt (FOV) Race 4 (y axis scale from 0 to 5: 0 = no symptoms and 5 = plant dead) on check cultivars and elite germplasm lines from 13 public breeding/genetics programs from 10 U.S. states: Arkansas, South Carolina, Georgia, Mississippi, Louisiana, Alabama, New Mexico, Texas, North Carolina, and California. One independent replicated field evaluation was conducted in California in 2011 for FOV Race 4 at the Kern County site, planted 27 Apr. 2011.

In 2008, the VRS and PS values for FOV Race 4 of susceptible check Pima S-7 were 4.4 and 5.1% for the FCA08_FOVR4 Fresno County field site and 3.0 and 6% for the KCA08_ FOVR4 Kern County field site. For the susceptible check Phytogen 72, VRS and PS values were 2.6 and 60% for the Fresno County and 2.1 and 26% for the Kern County sites (Fig. 1 and 2). At the KCA10_FOVR4 field site in 2010, the VRS and PS values of FOV Race 4 were 2.9 and 45.1%, respectively, for Pima S-7 and 1.9 and 84.7%, respectively, for Phytogen 72. In addition, no correlation or association was observed for VRS values of infection between FOV Race 1 + RKN and FOV Race 4 in either 2008 or 2010 evaluations. In 2011, a similar response for FOV Race 1 + RKN and FOV Race 4 (Fig. 3 and 4) infection was observed on tolerant or resistant (VRS £ 2.0 and PS ³ 80%) and susceptible (VRS > 2.0 and PS £ 80%) check cultivars. In 2008 at the FCA08_FOVR4 and KCA08_FOVR4 field sites, VRS values of FOV Race 4 infection were significantly 1640

correlated between the two infested evaluation field sites, with r = 0.58 at P £ 0.05. A correlation was also observed between the two sites for PS (r = 0.37) at P £ 0.05, indicating overall similarity in the responses of the evaluated lines at both FOV Race 4 sites. Averages for VRS and PS were 2.10 and 55% (FCA08_FOVR4) and 2.0 and 61% (KCA08_FOVR4). In 2008, VRS and PS values of infection for FOV Race 4 at the two sites were also negatively correlated, ranging from r = –0.34 (KCA08_FOVR4) to r = –0.68 (FCA08_FOVR4). In 2010, VRS and PS were also negatively correlated, with r = –0.64 (KCA10_FOVR4) at P £ 0.05. These correlations also indicated that a high VRS value resulted in low PS. Similar results were obtained for elite germplasm lines when comparing infested field evaluation sites (FOV Race 1 + RKN [Shafter site] and FOV Race 4 [Kern and Fresno counties]) (Table 2). For example, in 2008, we observed that AU-5491 (Alabama), Ark0008-22-10 (Arkansas), and LA05307061 (Louisiana) responded differently to the two races based on Agronomy Journal • Volume 105, Issue 6 • 2013

Fig. 4. Distribution of field plant survival (y axis scale from 0 to 100%) of check cultivars and elite germplasm lines from 13 public breeding/genetics programs from 10 U.S. states: : Arkansas, South Carolina, Georgia, Mississippi, Louisiana, Alabama, New Mexico, Texas, North Carolina, and California. Plant death was assumed to be due to disease infection of Fusarium wilt (FOV) Race 4. One independent replicated field evaluation conducted in California in 2011 for FOV Race 4 at the Kern County site, planted 27 Apr. 2011.

VRS values. Each was more susceptible to Race 4 than Race 1 + RKN (Fig. 1 and 2). In addition, in 2010, we observed that GA2006053 (Georgia), MD51ne (Mississippi), and 0033-6 (Mississippi) were more susceptible to FOV Race 1 + RKN than to FOV Race 4 (data not presented). In 2010, VRS and PS values on elite germplasm for FOV Races 1 and 4 infections were lower (possibly due to different inoculum levels in the field) than in 2008; however, cultivar resistance and susceptible checks for the two races responded as expected in 2010, with high VRS and low PS values similar to 2008 observations. Entries AU-6103 (Alabama), Ark0015-06-11 (Arkansas), LA05307029 (Louisiana), and 0149-17ne and 04-PST-275 (Mississippi) appeared tolerant to both FOV races (1 and 4) based on VRS and PS values from the 2008 trials. Similar results were obtained in 2010, when some elite germplasm lines from Alabama (AU6001), Arkansas (Ark0203-11), Louisiana (LA07307106), Mississippi (MD25Y), and South Carolina (PX03201-66-1) also appeared to be tolerant to both FOV races (data not presented). Other germplasm lines appeared tolerant in terms of good growth rates, lack of visual foliar symptoms, and high PS but still showed high infection rates as evidenced by high VRS values (Fig. 1 and 2). In 2008, >50% of the germplasm lines had a VRS for FOV Race 1 + RKN ³ 1.4 and a PS £ 85%, while for FOV Race 4, >50% of the germplasm lines had a VRS of ³ 2.0 and a PS £ 65% at least at one site (Fig. 1 and 2). In 2010, >30% of the germplasm lines had a VRS for FOV Race 4 ³ 1.5 and a PS £ 92%, while for FOV Race 1 + RKN they had a VRS ³ 1.0 and a PS £ 87% (data not presented). In 2011, many upland lines were severely affected by FOV at the field test site (KCA11_ FOVR4). Fusarium wilt Race 4 has been the more devastating race for cotton in California; VRS values ranged from 1.1 to 2.5 for the elite germplasm lines, with resistant Pima S-6 = 0.6, susceptible Pima S-7 = 4.5, and Phytogen 72 = 2.6 (Fig. 3). Plant survival ranged from 58 to 91% for the elite germplasm lines, with resistant Pima S-6 = 95%, susceptible Pima S-7 = 8%, and Phytogen 72 = 46% (Fig. 4).

Based on these evaluations to date, many of the entries in the current RBTN public elite upland germplasm pool may be more susceptible than expected to some FOV races, and sources of acceptable levels of resistance may be limited when tested under infestation levels that resulted in only 5 to 35% plant survival in susceptible check cultivars. Yield and Fiber Quality Evaluations When the performance of the elite germplasm lines was evaluated under SJV environments on non-FOV-infested fields for yield potential and fiber quality characteristics, significant variation (P £ 0.05) was observed among elite germplasm lines and check cultivars for agronomic (seed cotton yield, lint yield, and lint percentage) and fiber quality traits (fiber length (upper half mean), fiber strength, fiber elongation, micronaire, short fiber content, short fibers by weight, nep size, upper quartile fiber length, fiber length, seed coat fragment size, fiber fineness, immature fiber content, and maturity ratio) during 2 yr (2010 and 2011) at the University of California West Side Research and Extension Center, Five Points, CA (WSCA10- 11_YnF) and Shafter Cotton Research Station, Shafter, CA (SCA11_ YnF) (Table 2). Genotype ´ site interaction was significant (P £ 0.05) for agronomic and fiber quality traits, except for lint percentage and fiber strength. In the test at the SCA10_YnF Shafter field site in 2010, correlations between agronomic traits on a mean basis were only significant between lint yield and lint percentage (r = 0.66) (Table 3). For fiber quality traits, fiber length was negatively correlated with micronaire (r = –0.54) and short fiber content (r = –0.43) and positively correlated with fiber strength (r = 0.75) at P £ 0.05. Fiber strength was negatively correlated with short fiber content (r = –0.56) (Table 3). In the test at the WSCA10_YnF West Side field site in 2010, lint percentage was positively correlated with micronaire (r = 0.39) (Table 3); fiber length was also negatively correlated with micronaire (r = –0.63) and positively correlated with fiber strength (r = 0.59). Fiber strength was also negatively correlated with short fiber content (r = –0.58) (Table 3). Similar correlations were


1641

Table 3. Agronomic and fiber trait correlations of high-volume instrument (HVI) tests in 2010. Cotton trait

Plot weight

Lint yield

Cotton Research Station, Shafter, CA Lint yield 0.88*** Lint percentage 0.24 0.66*** Fiber length –0.02 –0.17 Fiber strength –0.04 –0.17 Micronaire 0.09 0.19 Fiber elongation 0.36* 0.31 Short fiber content 0.19 0.27 University of California West Side Research Station, Five Points, CA Lint yield 0.95*** Lint percentage –0.18 0.11 Fiber length 0.22 0.16 Fiber strength –0.01 –0.06 Micronaire 0.01 0.11 Fiber elongation 0.34* 0.39* Short fiber content –0.37* –0.34*

Lint percentage

Fiber length

Fiber strength

Micronaire

Fiber elongation

–0.30 –0.27 0.24 0.07 0.25

0.75*** –0.54*** –0.02 –0.43**

–0.25 0.10 –0.56***

0.27 –0.14

–0.32

–0.33 –0.32 0.39* 0.17 0.18

0.59*** –0.63*** –0.03 –0.25

–0.43** 0.13 –0.58***

0.15 –0.10

–0.30

* Significant at P < 0.05. ** Significant at P < 0.01. *** Significant at P < 0.001.

Table 4. Agronomic and fiber trait correlations of high volume instrument (HVI) tests from the University of California West Side Research Station, Five Points, CA, in 2011. Cotton trait Lint yield Lint percentage Fiber strength Micronaire Fiber elongation Short fiber content

Plot weight 0.83*** –0.10 0.17 –0.04 0.01 –0.15

Lint yield

Lint percentage

Fiber length

Fiber strength

Micronaire

Fiber elongation

0.30*** 0.01 0.25** 0.20* –0.10

–0.42*** 0.53*** 0.26** 0.24**

0.52*** –0.51*** –0.35*** –0.44***

–0.41*** –0.15* –0.55***

0.18* 0.12

–0.04

* Significant at P < 0.05. ** Significant at P < 0.01. *** Significant at P < 0.001.

observed for fiber length and fiber strength in 2011 at the WSC11_YnF field site (Table 4). When we analyzed the data on fiber quality traits obtained by AFIS in 2011, nep size and seed coat fragment size were positively correlated (r = 0.29) as well as fiber fineness the and maturity ratio (r = 0.67) (Table 5). Fiber fineness was negatively correlated with short fiber weight (r = –0.45), upper quartile fiber length (r = –0.38), and 5% fiber length (r = –0.43). Immature fiber content was negatively correlated with fiber fineness (r = –0.64) and positively correlated with short fiber weight (r = 0.70) at P £ 0.05 (Table 5). Some of the elite germplasm lines from the public breeders’ gene pools were observed to have moderate to good levels of resistance to FOV Race 1 or 4 or both and produced lint yields comparable to or better than standard Acala upland cultivars such as Phytogen 72 currently grown in the SJV of California (data not presented); however, some of these germplasm lines also possessed weak (low strength) and coarse (high micronaire) fibers under California environments. The above negative correlations of micronaire and fiber fineness with some fiber traits are indicators of positive effect. The longer the fiber, the finer the fiber may be, but at the same time it could be an indicator that some of the lines possess a higher number of immature fibers, which affects the dyeing process of these fibers 1642

(Ulloa, 2006). A similar negative correlation (r = –0.87) was observed for fiber traits of the elite germplasm lines between maturity ratio and immature fiber content (Table 5). Discussion In this study, a series of evaluations were conducted to assess FOV resistance in elite upland cotton germplasm lines from 13 public breeding programs across the Cotton Belt of the United States. Germplasm lines were evaluated on field sites infested with FOV Race 1 + RKN and FOV Race 4. The results revealed interactions in disease response between the assayed elite germplasm lines, FOV races (1 and 4), and evaluation sites (Fig. 1–4). When resistant cotton cultivars or germplasm from different genetic backgrounds are challenged by different races with different geographic origins, they may not express similar modes of inheritance of resistance (Ulloa et al., 2013). In field evaluation trials, differences in host-plant response may also be confounded by inoculum densities, pathogen distribution in the field, or differences in the environment, such as stress conditions during the growing season. In this study, several elite germplasm lines tolerant to FOV infection were identified from the breeders’ genetic pool represented in the RBTN. The lines were observed to have good levels of resistance to FOV Agronomy Journal • Volume 105, Issue 6 • 2013

Table 5. Fiber trait correlations of the advanced fiber information system (AFIS) from the University of California West Side Research Station, Five Points, CA, in 2011. Cotton trait Nep size UQ fiber length 5% Fiber span length Seed coat fragment size Fiber fineness Immature fiber content Maturity ratio

Short fiber content

Nep size

UQ† fiber length

–0.14 –0.12 –0.06 –0.08 –0.45*** 0.70*** –0.55***

0.16 0.13 0.29*** –0.02 –0.14 0.06

0.98*** –0.04 –0.38*** 0.05 –0.08

5% Fiber span Seed coat length fragment size

–0.06 –0.43*** 0.06 –0.08

0.21* –0.16 0.10

Fiber fineness

Immature fiber content

–0.64*** 0.63***

–0.87***

* Significant at P < 0.05. *** Significant at P < 0.001. † UQ, upper quartile.

Races 1 or 4 or both and produced good lint yield compared with Phytogen 72, an Acala cultivar grown widely in the SJV of California; however, some of these germplasm lines also possessed weaker (low strength) and coarse (high micronaire) fibers under California environments. Further optimization of phenotyping is needed to improve plant-resistance evaluations to minimize environmental variation and to increase resistance expression in segregating progeny. Additional breeding and selection are necessary to improve fiber quality in some of these germplasm lines. Continued development of cotton germplasm with wide adaptability and improved host-plant resistance with enhanced fiber quality is essential for the long-term survival of the U.S. cotton industry. In addition, continuing the introduction of genetic diversity into cultivated plants is important for reducing crop vulnerability (Ulloa et al., 2009). Pedigree information on the elite germplasm lines from the RBTN group revealed that breeders for the most part used in-house germplasm, germplasm developed from crosses derived from obsolete germplasm deposited in the USDA-ARS Cotton Germplasm Collection, germplasm developed from crosses derived from germplasm obtained from other breeders, and germplasm developed from crosses derived from elite commercial cultivars. The most common obsolete commercial cultivars and public germplasm used as parents in different crosses to derive the elite germplasm lines of the RBTN group included: SureGrow 747, DP (491, 493, and 565), DeltaPearl, Fiber Max (958, 966, 989), PSC (161 and 355), LA877, and DES199. Elite lines such as AU6001 and AU6103 that appeared to be tolerant to FOV races were derived from a cross between Miscot 8001 and SureGrow 747, while Ark0015-06-11 was derived from a cross between the Ark9308-14 and Ark9101 advanced breeding lines. This line was later publically released as Arkot0015b (Bourland and Jones, 2011a). Additional elite lines have been publically released from the RBTN group, e.g., Arkot 008, 009, and 0012 (Bourland and Jones, 2011b), TAM B182-34 (Smith et al., 2009), and Tamcot 73 (Smith et al., 2011). Integrating disease resistance, into high-yielding, high-fiberquality cultivars continues to be one of primary objectives of many breeding programs. Results from our studies identified genetic sources of FOV resistance that could be useful to breeders for cotton improvement; however, the F. oxysporum f. sp. vasinfectum pathogenicity mechanisms and the inheritance of FOV resistance genes differ significantly among FOV races for cotton genotypes (Ulloa et al., 2013). Differences in resistance

responses of elite germplasm lines to FOV Races 1 and 4 were observed when VRS and PS values of disease severity were compared from infested field evaluation sites (FOV Race 1 + RKN [Shafter site] and FOV Race 4 [Kern and Fresno counties]) (Fig. 1 and 2). When breeding for FOV resistance, it is important to document and identify the specific race or races to conduct the appropriate breeding selection scheme and to identify the appropriate molecular markers for applying marker-assisted selection to introgress, combine, or deploy individual genes for FOV resistance in developing cultivars (Ulloa et al., 2013). Acknowledgments We would like to acknowledge the assistance of University of California Cooperative Extension Farm Advisors (Dan Munk, Fresno County, and Brian Marsh, Kern County). Special thanks for field project support provided by Monica Biggs, Zulema Garcia (formerly USDA-ARS, Shafter Cotton Research Station), Mark Keeley, Raul Delgado, Gerardo Banuelos, and many student and research assistants from the University of California County Cooperative Extension and Research and Extension Centers, and USDA-ARS, WICSRU. Access to field sites was made possible with the permission and generous assistance of growers. We also thank Cotton Incorporated, Cary, NC, the California State Support Committee of Cotton Incorporated, the California Cotton Alliance, and the Cotton Foundation for partial support of this study. Mention of trade names or commercial products is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA or the University of California. The USDA and the University of California are equal opportunity providers and employers. References Armstrong, G.M., and J.K. Armstrong. 1960. American, Egyptian, and Indian cotton-wilt fusaria: Their pathogenicity and relationship to other wilt fusaria. USDA Tech. Bull. 219. U.S. Gov. Print. Office, Washington, DC. Armstrong, G.M., and J.K. Armstrong. 1978. A new race (Race 6) of the cotton-wilt Fusarium from Brazil. Plant Dis. Rep. 62:421–423. Armstrong, J.K., and G.M. Armstrong. 1958. A race of the cotton wilt Fusarium causing wilt of Yelredo soybean and flue-cured tobacco. Plant Dis. Rep. 42:147–151. Becerra, L.A., V.J. Lopez-Lavalle, V.J. Gillespie, W.A. Tate, M.H. Ellis, W.N. Stiller, et al. 2012. Molecular mapping of new sources of Fusarium wilt resistance in tetraploid cotton (Gossypium hirsutum L.). Mol. Breed. 30:1181–1191. doi:10.1007/s11032-012-9705-z Bell, A.A. 1984. Cotton protection practices in the USA and world. Section B: Diseases. In: R.J. Kohel and C.F. Lewis, editors, Cotton. Agron. Monogr. 24. ASA, CSSA, and SSSA, Madison, WI. p. 288–309. doi:10.2134/ agronmonogr24.c9


1643

Bourland, F.M., and D.C. Jones. 2011a. Registration of Arkot 0015a, Arkot 0015b, and Arkot 0016 germplasm lines of cotton. J. Plant Regist. 5:379– 383. doi:10.3198/jpr2010.12.0704crg Bourland, F.M., and D.C. Jones. 2011b. Registration of Arkot 0008, Arkot 0009, and Arkot 0012 germplasm lines of cotton. J. Plant Regist. 5:379– 383. doi:10.3198/jpr2010.12.0704crg DeVay, J.E. 1986. Half a century dynamics and control of cotton diseases: Fusarium and Verticillium wilts. In: Proceedings of the Beltwide Cotton Production Research Conferences, Las Vegas, NV. 4–9 Jan. 1986. Natl. Cotton Counc. Am., Memphis, TN. p. 35–41. Garber, R.H., E.C.C. Jorgenson, S. Smith, and A.H. Hyer. 1979. Interaction of population levels of Fusarium oxysporum f.sp. vasinfectum and Meloidogyne incognita on cotton. J. Nematol. 11:33–37. Garber, R.H., and G.A. Paxman. 1963. Fusarium wilt of cotton in California. Plant Dis. Rep. 47:398–400. Heald, C.M., and C.C. Orr. 1982. Nematode parasites of cotton. In: W.R. Nickle, editor, Plant and insect nematodes. Marcel Dekker, New York. Holmes, E.A., R.S. Bennett, D.W. Spurgeon, P.D. Colyer, and R.M. Davis. 2009. New genotypes of Fusarium oxysporum f. sp. vasinfectum from the southeastern United States. Plant Dis. 93:1298–1304. doi:10.1094/ PDIS-93-12-1298 Hutmacher, R.B., M. Ulloa, S.D. Wright, R.M. Davis, M.P. Keeley, and R. Delgado, et al. 2011. Fusarium Race 4: Management recommendations for growers. In: Proceedings of the Beltwide Cotton Conferences, Atlanta, GA. 4–7 Jan. 2011. Natl. Cotton Counc. Am., Memphis, TN. p. 188–192. Ibrahim, F.M. 1966. A new race of the cotton-wilt Fusarium in the Sudan Gezira. Emp. Cotton Grow. Rev. 43:296–299. Kim, Y., R.B. Hutmacher, and R.M. Davis. 2005. Characterization of California isolates of Fusarium oxysporum f. sp. vasinfectum. Plant Dis. 89:366– 372. doi:10.1094/PD-89-0366 Kochman, J., L. Swan, N. Moore, S. Bentley, W. O’Neill, A. Mitchell, et al. 2002. The Fusarium threat: Are we making the progress? In: Proceedings of the 11th Australian Cotton Conference, Brisbane, QLD, Australia. 13–15 Aug. 2002. Aust. Cotton Growers’ Res. Assoc., Wee Waa, NSW, Australia. p. 643–652. Mohamed, H.A. 1963. Inheritance of resistance to Fusarium wilt in some Egyptian cottons. Emp. Cotton Grow. Rev. 40:292–295. Ott, L. 1988. An introduction to statistical methods and data analysis. PWSKent Publ. Co., Boston. Sasser, J.N. 1972. Nematode disease of cotton. In: J.M. Webster, editor, Economic nematology. Academic Press, New York. p. 187–214. Skovgaard, K., H.I. Nirenberg, K. O’Donnell, and S. Rosendahl. 2001. Evolution of Fusarium oxysporum f. sp vasinfectum races inferred from multigene genealogies. Phytopathology 91:1231–1237. doi:10.1094/ PHYTO.2001.91.12.1231 Smith, A.L., and J.B. Dick. 1960. Inheritance of resistance to Fusarium wilt in upland and Sea Island cotton as complicated by nematodes under field conditions. Phytopathology 50:44–48.

1644

Smith, C.W., R.G. Cantrell, H.S. Moser, and S.R. Oakley. 1999. History of cultivar development in the United States. In: C.W. Smith and J. Cothren, editors, Cotton: Origin, history, technology, and production. John Wiley & Sons, New York. p. 99–171. Smith, C.W., S. Hague, and D. Jones. 2011. Registration of ‘Tamcot 73’ upland cotton cultivar. J. Plant Regist. 5:273–278. doi:10.3198/ jpr2010.12.0723crc Smith, C.W., S. Hague, P.S. Thaxton, E. Hequet, and D. Jones. 2009. Registration of eight extra-long staple upland cotton germplasm lines. J. Plant Regist. 3:81–85. doi:10.3198/jpr2008.02.0114crg Turcotte, E.L., R.G. Percy, and C.F. Feaster. 1992. Registration of ‘Pima S-7’ American Pima cotton. Crop Sci. 32:1291. doi:10.2135/cropsci1992.00 11183X003200050047x Ulloa, M. 2006. Heritability and correlations of agronomic and fiber traits in an okra-leaf upland cotton population. Crop Sci. 46:1508–1514. doi:10.2135/cropsci2005.08-0271 Ulloa, M., C. Brubaker, and P. Chee. 2007. Cotton. In: C. Kole, editor, Genome mapping and molecular breeding. Vol. 6. Technical crops. Springer-Verlag, Heidelberg, Germany. p. 1–49. doi:10.1007/978-3-540-34538-1_1 Ulloa, M., R.B. Hutmacher, R.M. Davis, S.D. Wright, R. Percy, and B. Marsh. 2006. Breeding for Fusarium wilt Race 4 resistance in cotton under field and greenhouse conditions. J. Cotton Sci. 10:114–127. Ulloa, M., R.B. Hutmacher, P.A. Roberts, S.D. Wright, R.L. Nichols, and R.M. Davis. 2013. Inheritance and QTL mapping of Fusarium wilt Race 4 resistance in cotton. Theor. Appl. Genet. 126:1405–1418. doi:10.1007/ s00122-013-2061-5 Ulloa, M., R.B. Hutmacher, S.D. Wright, B. Campbell, T. Wallace, G. Myers, et al. 2010. Beltwides’ elite upland germplasm pool assessment of Fusarium wilt (FOV) Races 1 and 4 in California. In: Proceedings of the Beltwide Cotton Conferences, New Orleans, LA. 4–7 Jan. 2010. Natl. Cotton Counc. Am, Memphis, TN. p. 765–766. Ulloa, M., R. Percy, J. Zhang, R.B. Hutmacher, S.D. Wright, and R.M. Davis. 2009. Registration of four Pima cotton germplasm lines having good levels of Fusarium wilt Race 4 resistance with moderate yields and good fibers. J. Plant Regist. 3:198–202. doi:10.3198/jpr2008.09.0530crg Ulloa, M., C. Wang, R.B. Hutmacher, S.D. Wright, R.M. Davis, C.A. Saski, and P.A. Roberts. 2011. Mapping Fusarium wilt Race 1 resistance genes in cotton by inheritance, QTL, and sequencing composition. Mol. Genet. Genomics 286:21–36. doi:10.1007/s00438-011-0616-1 Veech, J.A. 1984. Cotton protection practices in the USA and world. Section C: Nematodes. In: R.J. Kohel and C.F. Lewis, editors, Cotton. Agron. Monogr. 24. ASA, CSSA, and SSSA, Madison, WI. p. 309–329. doi:10.2134/agronmonogr24.c9 Wang, B., C.L. Brubaker, and J. Burdon. 2004. Fusarium species and Fusarium wilt pathogens associated with native Gossypium populations in Australia. Mycol. Res. 108:35–44. doi:10.1017/S0953756203008803 Wang, P., L. Su, L. Qin, B. Hu, W. Guo, and T. Zhang. 2009. Identification and molecular mapping of Fusarium wilt resistant gene in upland cotton. Theor. Appl. Genet. 119:733–739. doi:10.1007/s00122-009-1084-4
