Compendium of Rose Diseases and Pests, Second Edition by Scientific Societies

Compendium of Rose Diseases and Pests SECOND EDITION

R. Kenneth Horst Cornell University Ithaca, NY

Raymond A. Cloyd Kansas State University Manhattan, KS

The American Phytopathological Society

Whatâ&#x20AC;&#x2122;s in a name? That which we call a rose By any other name would smell as sweet Shakespeare, Romeo and Juliet

Cover photographs by Steve Kronmiller Library of Congress Control Number: 2007927277 International Standard Book Number: 978-0-89054-355-9 ÂŠ 2007 by The American Phytopathological Society First edition published 1983 Second edition published 2007 All rights reserved. No portion of this book may be reproduced in any form, including photocopy, microfilm, information storage and retrieval system, computer database, or software, or by any means, including electronic or mechanical, without written permission from the publisher. Printed in China on acid-free paper. The American Phytopathological Society 3340 Pilot Knob Road St. Paul, Minnesota 55121, U.S.A.

To Dr. Cynthia Westcott (1898–1983), “The Plant Doctor,” a pioneer leader in plant pathology, and author of Anyone Can Grow Roses. Her greatest enthusiasm was always the rose.

Preface R. W. Langhans, Cornell University, Ithaca, NY K. Milne, Massey University, Palmerston North, New Zealand L. W. Moore, Oregon State University, Corvallis, OR L. P. Nichols (deceased) G. Nyland, University of California, Davis, CA K. Ohkawa, Kanagawa-Ken, Japan N. Paludan, The State Plant Pathology Institute, Lyngby, Denmark U. Paz, Ministry of Agriculture, Hedera Region, Israel C. C. Powell, Plant Health Advisory Services, Worthington, OH M. Rice, Iowa State University, Ames, IA M. N. Rogers, University of Missouri, Columbia, MO R. Rosetta, Oregon State University, Corvallis, OR G. A. Secor, North Dakota State University, Fargo, ND J. G. Seeley (retired), Ithaca, NY D. J. Shetlar, Ohio State University, Columbus, OH L. L. Stubbs, University of Melbourne, Parkville, Victoria, Australia B. J. Thomas, Glasshouse Crops Research Institute, Littlehampton, England P. T. Tiddens, Chicago Botanic Garden, Glencoe, IL V. A. Wager, South African Garden & Home, Durban, South Africa K. Welch, University of California, Berkeley, CA

The Compendium of Rose Diseases was the first in The American Phytopathological Society’s series of disease compendia to cover diseases of a commercial flowering ornamental. That compendium has been revised, updated, expanded, and given a new format, with color throughout. The primary purpose of Compendium of Rose Diseases and Pests, Second Edition is to aid plant pathologists and other agricultural workers in the diagnosis of rose diseases. It is also designed to serve as a practical reference and resource for rose growers, students, researchers, educators, crop disease consultants, advisors in state and federal government and regulatory agencies, agribusiness representatives, the pest control industry, county agricultural and cooperative extension agents, and area crop specialists throughout the world. The compendium is amply illustrated and uses descriptive terminology. Diseases are arranged according to causal agents; infectious diseases, caused by fungi, bacteria, viruses, and nematodes, are covered first, followed by noninfectious diseases, including physiologic problems, environmental imbalances, air pollution, pesticide toxicity, and nutritional deficiencies and toxicities. Insect and mite pests are also included in this second edition. An appendix, glossary, index, and selected references are included. The references cited in each section were selected to include the most contemporary literature applicable to the discussion of the pests and diseases and thus are not all-inclusive. Discussions of pest and disease management measures purposely stress principles and cultural practices that are not likely to become obsolete. For specific information concerning chemi cal control measures, the reader should consult recent literature and extension or advisory plant pathologists. Comments regarding the general usefulness of or omissions in this compendium are most welcome. With your suggestions, future editions can be made even more useful and practical. The authors thank the following individuals, who reviewed all or part of the manuscript, made numerous valuable suggestions, and contributed images.

The Department of Plant Pathology at Cornell University provided office, library, and communication facilities and secretarial and photographic services and support. The stenographic expertise of Margaret Haus and her patience and attention to detail in manuscript preparation were invaluable. The professional photographic expertise of H. H. Lyon and Kent Loeffler are gratefully acknowledged. Carl Whittaker prepared illustrations of life cycles and drawings of fungal fruiting structures, and R. P. Korf and K. Hodge provided valuable advice in the mycological area. The help of Marlin N. Rogers, University of Missouri, who wrote the section on noninfectious diseases, is greatly appreciated. Without the assistance of The Fred C. Gloeckner Foundation, the project could not have been completed. The invaluable aid and support of J. Shibata, Cherry City Nursery and California-Florida Plant Corporation, in preparing illustrations used in the compendium are gratefully acknowledged. Unless otherwise indicated in the caption, images are courtesy of the Department of Plant Pathology, Cornell University.

R. Brewer, University of California, San Joaquin, CA D. L. Coyier, Oregon State University, Corvallis, OR W. S. Cranshaw, Colorado State University, Fort Collins, CO O. W. Davidson, Rutgers University, New Brunswick, NJ P. Fry, Massey University, Palmerston North, New Zealand F. A. Hakkaart, Research Station for Floriculture, Aalsmeer, the Netherlands E. L. Halk, USDA-ARS, Beltsville, MD M. B. Harrison (retired), San Diego, CA C. Harwood, Bear Creek Gardens, Medford, OR

R. Kenneth Horst Raymond A. Cloyd

Contents Introduction

Part II. Noninfectious Diseases

1 1 1 2 2 3 3

43 43 43 44 44 44 44 45 45 45 45 46 46 46 46 47 49 50

Rose Parentage/Hybrids Cultivar Classification General Maintenance/Production Practices Rose Diseases Infectious Diseases Noninfectious Diseases/Disorders Disease and Pest Management

Part I. Infectious Diseases 5 5 8 12 15 16 18 19 20 21 21 24 25 28 28 30 32 32 34 35 35 36 37 37 38 39 39 39 40

Diseases Caused by Fungi Powdery Mildew Black Spot Rust Verticillium Wilt Downy Mildew Brand Canker Common Canker (Rose Graft Canker) Brown Canker Black Mold Botrytis Blight Canker (Dieback) Miscellaneous Diseases Caused by Fungi Diseases Caused by Bacteria Crown Gall Hairy Root Diseases Caused by Viruses or Graft Transmissible Organisms Rose Mosaic Strawberry Latent Ringspot Rose Streak Rose Rosette Rose Ring Pattern Rose Wilt Rose Spring Dwarf Rose Leaf Curl Rose Flower Break Rose Flower Proliferation Tobacco Streak Diseases Caused by Nematodes

Physiologic Problems Blindness Bullheads Bent Neck (Vascular Occlusion) Environmental Imbalances Petal Blackening in ‘Baccara’ Roses Petal Bluing in ‘Baccara’ Roses Heat and Moisture Stress Oxygen Deficiency Air Pollution Fluoride Ethylene Mercury Vapor Paint Volatiles Pesticide Toxicity Nutritional Deficiencies Nutritional Toxicities Salinity

Part III. Insect and Mite Pests 51 52 54 56 58 59 60 61 61 62 62 63

Rose Aphid Japanese Beetle Twospotted Spider Mite Rose Midge Rose Sawfly Flower Thrips Rose Leafhopper Rose Chafer Rose Curculio Fuller Rose Beetle Western Flower Thrips Miscellaneous Rose Pests

67 Appendix 71 Glossary 79 Index

vii

Compendium of Rose Diseases and Pests SECOND EDITION

Introduction The rose is the most popular garden plant in the world as well as the most important commercial cut flower grown under glass. From 1970 to 1980, commercial cut flower roses in the United States exceeded all other cut flowers in wholesale value. In 1970, the wholesale value of roses was $54 million; by 1980, the whole sale value had nearly doubled to $105.7 million. By 2003, the wholesale value of both cut roses and potted roses declined to $79.2 million. This reduction in the wholesale value of roses in the United States is best understood by looking at the wholesale value of imported roses. Whereas, the wholesale value of roses imported into the United States in 1980 was $11 million, the wholesale value of roses imported into the United States in 2002 was $122.5 million from Colombia and $53.0 million from Ecua dor. By 2003, the wholesale value of roses imported from Colom bia was $144.8 million and from Ecuador was $59.7 million. The modern cultivated rose in the genus Rosa is a monument to the achievements of practical plant breeders. The genus has differentiated into at least 200 botanical species widely distrib uted in the Northern Hemisphere. All members of the genus are important in horticulture for blooms as well as for ornamental plantings. Fossil specimens indicate the presence of primitive roses in Colorado and Oregon more than 30 million years ago. There is evidence that roses were first cultivated 4,000–5,000 years ago in northern Africa. The active speciation that has occurred since these early roses has given rise to many groups and hy brids that are difficult to separate taxonomically. The origin of the modern cultivated rose is shown in Figure 1A.

Rose Parentage/Hybrids Hybrid perpetual roses are of mixed ancestry; Rosa × bor boniana N. H. F. Desp. is the prevailing species. These culti vars have upright growth and produce large, fragrant, double flowers in early summer and sparingly in the fall. Most hybrid perpetual cultivars are hardy to the northern United States. Hybrid tea roses are mostly R. dilecta Rehder and represent crosses between hybrid perpetuals and virtually all other rose groups. They are not as hardy as hybrid perpetuals. Hybrid teas have a recurrent and fragrant blooming habit and are a pre dominant garden and greenhouse rose. Polyantha roses, an important branch of the multiflora class, are a cross between R. multiflora and R. chinensis, correctly known botanically as R. × rehderiana Blackburn. This group includes dwarf roses, which are sometimes called “baby ram blers”, and a subgroup that because of its blooming habit has been commercially called floribunda. Tea roses are principally R. odorata (Andrews) Sweet and are used much less as a group than are the hybrid teas. This group is noted for its abundance of large flowers but is not reli ably hardy north of the Mason-Dixon line in the United States. China and Bengal roses are essentially R. chinensis Jacq. and R. odorata (Andrews) Sweet, and their hybrids are used

in much the same way as are tea roses. Some are hardy in the central United States. The blooms are generally small and red. Noisette or Champney roses are hybrids of R. × noisettiana Thory. These excellent bush roses are not reliably hardy north of the Mason-Dixon line. This group is grown extensively in Europe. Multiflora roses are R. multiflora Thunb. ex Murray and in clude climbing roses, which are often called “ramblers”. The true multiflora roses have flower clusters. Wichuraiana roses are R. wichuraiana Crép. and are also called memorial roses. These roses are more or less evergreen and are ground trailers. They are a dominant form of hardy climbing rose and are difficult to distinguish from multiflora roses. Manetti is not considered a group of roses but must be men tioned since it is often used as an understock for grafted roses. Its origin is somewhat confused, but older historical literature in dicates that it should be called R. manetti Bals.-Criv. ex Rivers. R. manetti is of hybrid origin and is possibly segregated from a population of R. chinensis. Manetti is generally known to be tolerant of shallow or dry soils and of confined root systems. Interspecific hybridization is very important in the origin of modern rose types. Most cultivated roses are derived from hy brids involving several different wild species of roses. However, serious technical difficulties caused by sterilities from species of 2x, 3x, 4x, 5x, 6x, and 8x chromosomal constituencies have prevented the full utilization of the 200 or more species of the genus Rosa. Advances in molecular genetics should greatly aid in overcoming this problem and should allow the rapid develop ment of improved cultivars of roses in the future.

Cultivar Classification The system of cultivar classification has become complicated and inexact as hybridization has proceeded. Selection and hy bridization have given rise to thousands of cultivars. Modern Roses XI: The World Encyclopedia of Roses, published by Academic Press under the auspices of the American Rose So ciety (the international registration authority for roses), contains descriptions for more than 25,000 rose cultivars. The World Federation of Rose Societies and many of its member countries has accepted a classification system based on growth habit and flowering habit. The system uses a family tree divided first into three major groups: species roses, old garden roses, and mod ern roses (Fig. 1B). The subdivisions within each group are based on growth and bloom types.

General Maintenance/ Production Practices Pruning is necessary to obtain good roses. In cold climates, winter injury necessitates pruning in the spring to remove dead 1

Fig. 1. A, Rose genealogy. The origin of the modern cultivated rose as adapted from Stewart’s work (as described in Cairns et al., 2000). B, The genus Rosa family tree.

wood and poor, weak cane growth. In milder climates, dead wood and weak wood are also removed, depending on the size of plants desired. In general, pruning should be done in late winter or early spring, although some pruning may be neces sary during the summer to maintain plant appearance. Roses may be propagated by rooting cuttings, by budding, or by grafting. For the gardener, propagation by rooting cuttings is the most practical technique. The simplest method is to make 12-to 20-cm-long cuttings from stems that have just finished flowering. These cuttings are placed in the ground under a jar

in a shady location and kept moist at all times. Commercial nurseries propagate roses by budding onto an understock in the field. Many cultivars are more vigorous when budded on an understock than when grown on their own roots. Selected Reference Cairns, T. (ed.), Young, M. (assoc. ed.), Adams, J. (assoc. ed.), and Edberg, B. (assoc. ed.) 2000. Modern Roses XI: The World Ency clopedia of Roses. Academic Press, San Diego, CA.

Rose Diseases Infectious Diseases Infectious diseases are caused by fungi, bacteria, viruses, andnematodes.Diseasedevelopmentdependsonthepresence of a virulent pathogen, a susceptible host, and the proper en vironmental conditions. Disease symptoms may be classified as necrosis, or death of cells, tissues, or organs; hypoplasia, 2

resulting in dwarfing or stunting; or hyperplasia, resulting in an overgrowth of plant tissue, as found in crown gall.

Fungi Fungi are filamentous organisms that reproduce by sexual or asexual spores. More than 100,000 species of fungi have been described, of which about 20,000 species are patho

genic to plants, animals, or both. Fungi are usually identified by spore morphology and the mechanism of spore production, but advances in diagnostic techniques, such as serological and molecular-based techniques, have become increasingly com mon in fungal identification. Fungal spores are easily dis seminated by air currents, splashing water, and the activities of people; they can also move on or in plant parts or animals. Fungi overwinter on and in living or dead plants, in soil, and occasionally in insects.

Bacteria

Bacteria include some 4,000 prokaryotic species, most of which contain no chlorophyll. Several hundred species are pathogenic to plants, animals, or both. Plant-pathogenic bac teria are generally unicellular, non-spore-forming rods. The identification of bacteria can be very difficult; it involves spe cial staining techniques, biochemical tests, and serology. True bacteria in four families, Pseudomonadaceae, Enterobacte riaceae, Rhizobiaceae, and Mycobacteriaceae, cause plant disease. Only one of these families, Pseudomonadaceae, contain a single genus with species known to have significant pathogenicity to roses. The one genus with species pathogenic to roses is Agrobacterium. One other genus in this family has a species, Pseudomonas syringae van Hall pv. mors-prunorum (Wormald) Young et al., that has been reported to cause a dis ease called bacterial blast. However, the occurrence of this disease has not been commonly found on roses. In addition, Er winia amylovora (Burrill) Winslow et al., in the family Entero bacteriaceae, which causes fire blight on many plant species in the family Rosaceae, has been suggested to be pathogenic to roses; however, there is scant literature found to document that pathogenic association with roses. Bacteria enter plants through wounds, stomata, water pores (hydathodes), flower nectaries, and possibly lenticels. They can survive inactively for months in plant tissues and sometimes for years in soil. Bacteria are disseminated by people, insects, nematodes, splashing water, and windblown soil or sand. Free moisture and moderate to warm conditions are generally re quired for disease development.

Viruses and Organisms Associated with Viruslike Diseases

Six hundred or more plant diseases are thought to be caused by viruses; however, two-thirds of these have not been con clusively proved to have a viral causal agent. Viroids, phyto plasmas, and spiroplasmas have now been shown to cause some of these diseases, but the symptoms associated with the dis eases caused by these agents are similar to those associated with diseases known to be caused by viruses. Symptoms of viral diseases include suppression of chlorophyll production, leaf mottling, yellow or necrotic ring patterns in leaves, stunt ing, leaf and flower distortion, witches’-broom or rosettes, and sometimes necrosis. Viruses often contain two major components: (i) a nucleic acid encased in (ii) a protein coat. Viroids consist solely of a small amount of RNA with no protein coat. Viruses are differ entiated and identified by host specificity, physical properties, purification, electron microscopy, electrophoresis, serology, and molecular techniques. Viruses are transmitted by insects, mites, fungi, nematodes, mechanical means, grafting, dodder, and occasionally seeds. It is important to note that some of the diseases classified as a virus disease in this compendium, since they exhibit viruslike symptoms, have not yet been conclusively determined to have a viral causal agent. Mollicutes are some of the smallest free-living organisms known. Those that cause plant disease are commonly placed in two groups, phytoplasmas (formerly called mycoplasmalike organisms or MLOs) and spiroplasmas. Phytoplasmas are pleo morphic agents bounded by single membranes and devoid of cell walls and have not yet been cultured in vitro. Spiroplasmas

possess all the characteristics of phytoplasmas but, in addition, they have a distinct helical morphology and rotary and flexu ous motility and some have been cultured in vitro. Thus far, no viroids or spiroplasmas have been reported to be pathogens of roses; however, a phytoplasma has been associated with rose rosette disease, but causality has yet to be determined.

Nematodes

Nematodes are unsegmented roundworms that inhabit fresh and salt water, decaying organic matter, soil, plants, and animals throughout the world. More than 15,000 species of nematodes have been described, and about 2,200 species are parasitic on plants. Plant-parasitic nematodes are typically microscopic, transparent,mobile,andvermiform.Nematodesmovepassively in water, soil, and infected plant parts and on tools, vehicles, and machinery carrying infested soil; they are also dissemi nated by wind and many animals.

Noninfectious Diseases/Disorders Noninfectious disorders are caused by an excess, defi ciency, or imbalance of nutrients; by water, pH, and environ mental extremes; and by air pollutants, pesticides, and other injuries. Symptoms of noninfectious disorders may often be confused with diseases caused by fungi, bacteria, viruses, and nematodes.

Disease and Pest Management Control measures of a general nature are described for each disease covered in this compendium. Eliminating disease en tirely is not usually feasible, but economic control, such that the increased yield more than covers the cost of labor and ma terials, is quite possible. Disease and pest management may be achieved by a single procedure but more often involves the in tegrated use of several measures, often referred to as integrated pest management (IPM). The five fundamental principles of disease management are exclusion, eradication, protection, re sistance, and therapy. Exclusion means preventing pathogens from entering and becoming established in uninfested fields, gardens, states, or countries. To this end, commercial growers and gardeners should use plants certified to be free of selected diseases. States and countries often establish quarantines to exclude dangerous pathogens from entry. Eradication means the elimination of the pathogen once it has become established on plants in a field or garden. Eradi cation can be accomplished by removing diseased specimens, by rotating susceptible crops with nonsusceptible crops, and by disinfecting, usually with chemicals. Protection is the interposition of some protective barrier be tween the susceptible part of the host and the pathogen. In most instances, this requires protective sprays. Resistance refers to the development and use of cultivars that prevent or impede the activity of a pathogen. Although no single cultivar is resistant to all diseases, sources of resistance or tolerance to specific diseases can be used for control. Therapy is the treatment of plants with something that will inactivate or inhibit the pathogen. In chemotherapy, chemicals are used to inactivate the pathogen. Heat is sometimes used to inactivate or inhibit virus development in infected plant tissues so that newly developing tissue is free of the pathogen.

Integrated Pest Management

Cultural Practices. Cultural practices that are favorable to healthy plant growth should be used. (i) Dense plantings with 3

resultant wet leaves, for extensive periods of time, encourage thedevelopmentof foliar and cane fungal pathogens andshould be avoided. (ii) Improper pruning techniques provide wounds that encourage the invasion of pests and pathogens before a cal lus can form over the wound. Cane stubs, after pruning, should be no longer than 6 mm. (iii) Fallen leaves and dead canes, which are sources for continued disease and pest development, should be removed and destroyed. Biological Controls. Biological controls should be used when available and when appropriate. Chemical Controls. Biocompatible or minimum-risk chemi cals should be used as they become available. (i) Pesticides should be applied only when necessary. (ii) Application meth ods that apply less pesticide or a more efficient spray system should be used.

Five Basic Techniques for a Successful IPM Program

Scouting. Regular and random visual observations provide an early warning for insect, mite, and disease problems. Disease Identification. The first and most important step is to identify the problem. Misdiagnosis results in improper control. Timing. Improper timing of control measures results in dis ease or insect control failure. The control measure must be timed correctly to the stage of disease or insect development. Records. Accurate records are a good way to make appropri ate disease, insect, and mite control decisions. Labels and Material Safety Data Sheets (MSDS). Know, understand, and keep files on pesticide labels and MSDS that you use. All employees are protected by the Worker Protection Standard (WPS).

Part I. Infectious Diseases Diseases Caused by Fungi Powdery Mildew Powdery mildew is probably the most widely distributed and serious disease of greenhouse-, garden-, and field-grown roses. Although the causal fungus was first described in 1819, the disease was present long before then and is now known in all countries in which roses are grown.

Symptoms

Early symptoms are slightly raised, blisterlike, often red areas on the upper leaf surface. The white fungal growth, con sisting of mycelium and conidiophores, appears as discrete patches on the surface of young leaves, which become twisted and distorted as the powdery white growth completely covers them (Fig. 2). Older leaves may not be distorted, but circular or irregular areas may be covered with growth of the mildew fungus (Fig. 3). Mature leaves are not usually infected. When environmental conditions are favorable, the affected leaves may fall prematurely. Fungal growth may develop first on succulent, young stem tissues, especially at the base of thorns (Fig. 4). This growth persists when stems mature. On roses in landscape plantings,

Fig. 2. Leaf curl and distortion symptoms of powdery mildew, caused by Podosphaera pannosa. (Reprinted, by permission, from Horst, 2001)

the fungus, which is capable of overwintering in rudimentary leaves or bud scales, can readily infect new spring shoots that develop from these infected buds. The fungus may also attack the flowers and grow abundantly on the pedicels, sepals, and receptacles, especially when the flower bud is unopened (Fig. 5). This infection results in re duced flower quality. Severe mildew damage reduces leaf growth, aesthetic value of plants, photosynthetic efficiency and thereby plant growth, and salability of cut flowers. The number of flowers pro duced may also be reduced, but this has not been conclusively established.

Causal Organism Theophrastus (“The Father of Botany”) gave the first account of powdery mildew on roses around 300 b.c., but Wallroth in 1819 first described the fungus causing this disease as Alphito morpha pannosa. It was transferred to the genus Erysiphe as E. pannosa (Wallr.) Fr. in 1829 and finally was described and placed in the genus Sphaerotheca in 1851. Although the fungus has remained identified as S. pannosa (Wallr.:Fr.) Lév., some authorities recognize a division of this species by Woronichin

Fig. 3. Heavy, white mycelial growth of Podo sphaera pannosa, the cause of powdery mil dew, on upper leaf surfaces.

Fig. 4. Symptoms of powdery mildew, caused by Podosphaera pannosa, on a cane and thorns.

in 1914 into two varieties, S. pannosa var. rosae infecting rose and S. pannosa var. persicae infecting peach and almond. Some investigators believe that S. humuli (DC.) Burrill also occurs on roses and that most specimens from North America are S. humuli, whereas those from Europe are S. pannosa. Blumer in 1967 maintained this concept of two species caus ing powdery mildew on roses but identified the second fungus as S. macularis (Wallr.:Fr.) Lind, which is not considered by Salmon to be distinctly different from S. humuli. An extensive survey of fresh and herbarium material from around the world led Coyier to the determination that S. pannosa and S. humuli are not distinctly different and that powdery mildew on roses in the United States is caused by S. pannosa var. rosae. There is some evidence for biological specialization within S. pannosa. For example, S. pannosa from peach causes large necrotic le sions on apricot leaves, whereas S. pannosa from the rose cul tivar Dorothy Perkins causes small lesions on apricot leaves. It has been suggested, but not conclusively established, that there are five races of S. pannosa var. rosae based on pathogen viru lence and host susceptibility. With changes in fungal nomencla ture in recent years, the pathogen is now called Podosphaera pannosa. Isolates of the rose powdery mildew pathogen are not morphologically different from isolates found on Prunus spe cies (such as peach, almond, and apricot) and the “var. rosae” is no longer necessary. Some specialization may be found in which isolates from roses may be less damaging to Prunus spe cies and vice versa. After primary infections occur on roses, a secondary thick felt, called the “pannose mycelium”, is formed, from which the species gets its name. Ascocarps may be found within this my celium on some cultivars and are variously termed cleistocarps,

cleistothecia, or perithecia. Ascocarps are globose to pyriform and are 85–120 µm in diameter, with a few short, pale brown, mycelioid, septate appendages. Asci are broadly oblong to glo bose, measure 88–115 µm, and contain eight ascospores, each 12–15 × 20–27 µm. Ascocarps are formed somewhat erratically. In one area, they may form on some cultivars and not on others, and in other areas, they may not form consistently on any one cultivar. There is evidence from the early 1980s that P. pannosa is het erothallic. It is speculated that ascocarps, when formed, may provide a means of overwintering besides that of mycelium in dormant buds; however, little experimental evidence supports this conjecture, and investigators have been unable to get asco spores to germinate.

Disease Cycle

At 20°C and near 100% relative humidity, conidia begin to germinate 2–4 h after being deposited on the leaf. A short pri mary germ tube is produced from one side of the conidium (Fig. 6), and within 6 h, an appressorial initial is formed. From the bottom of the appressorium, a fine penetration tube pierces

Fig. 7. An electron micrograph showing mycelial growth and infec tion pegs of Podosphaera pannosa, the cause of powdery mildew, on a leaf surface.

Fig. 5. Mycelial growth of Podosphaera pannosa, the cause of pow dery mildew, on the calyx of a flower bud.

Fig. 6. Germinating conidia of Podosphaera pannosa, the cause of powdery mildew, on a leaf surface.

Fig. 8. Conidia of Podosphaera pannosa, the cause of powdery mildew, forming on the end of a conidiophore on a leaf surface.

the cuticle and enters the epidermal cell, where haustorial ini tials can be detected after 16–20 h. Further mycelial growth develops on the leaf surface (Fig. 7), and additional haustoria are formed in epidermal cells within 20–24 h. By 48 h, conidiophore initials form as swellings on hy phae immediately above the nuclei. Conidiophore initials elongate and nuclei divide, creating daughter nuclei, which pass into the initials; septa are then formed, which separate the initials and hyphae. Conidia averaging 22.9–28.6 µm long and 13.6–15.8 µm wide develop at the ends of conidiophores (Fig. 8). Successive conidia remain attached to each other in chains, giving the characteristic powdery appearance, or they may be broken off and carried to new infection sites by air cur rents (Fig. 9). Under optimal conditions, conidial chains are produced within 72 h after initial infection, although 5–7 days are normally required.

Conidia show a diurnal cycle of maturation and abstriction that leads to diurnal periodicity in the number of conidia in the air surrounding rose plants. On a rainless day, the number of conidia released increases as relative humidity decreases; num bers reach a peak from midday to early afternoon and decline as conidiophores are depleted of mature conidia. For roses grown outdoors in regions with severe winters, new infections are initiated from mycelia that overwinter in rudi mentary leaves of buds or in the inner bud scales, which survive because they are protected by the outer bud scales. When such buds develop, the resulting shoots become infected and cov ered with conidia. These conidia are airborne to newly forming leaves, where they initiate a new disease cycle. The fungus may also overwinter as ascocarps (Fig. 9); how ever, ascocarps are formed so erratically that this mechanism seems unlikely to be an effective means of overwintering.

Fig. 9. Powdery mildew disease cycle. A, Podosphaera pannosa overwinters in infected canes or buds and in fallen leaves. B, New shoots are infected from the overwintering mycelium or from conidia or ascospores produced on fallen leaves. C, Leaves and flowers are infected during the summer by airborne conidia or ascospores produced on infected portions of plants.

In mild climates and in greenhouses where growth of roses continues throughout the winter, no survival mechanism is needed, since conidia and new infection cycles are continually produced.

Epidemiology Differences in the susceptibility of rose cultivars to P. pan nosa have been reported. There are reports that ramblers, climbers, and hybrid teas are generally highly susceptible and that wichuraianas are more resistant; whereas other reports in dicate that floribunda and polyantha cultivars are more suscep tible than are hybrid teas. Furthermore, the growth stage of the host tissue at the time it becomes infected is important because the fungus grows well only on young (actively expanding) tis sues, with tissues becoming more resistant to infection as they age. Typically, the level of mildew development increases as new shoots develop and decreases as these shoots mature and terminate in flower buds. Termination in flower buds is fol lowed by a renewed increase in the level of powdery mildew as lateral buds break and new shoots develop. In addition to the susceptibility of host tissue, temperature, relative humidity, and presence of free water also have a strong influence on the growth of P. pannosa. The optimal tempera ture at high humidity is 21°C for conidium germination and 18–25°C for mycelial growth. The optimal relative humidity for the germination of conidia is 97–99%. In contrast, pow dery mildew development is adversely affected by the presence of films of water on the leaf surface. This effect is most pro nounced when leaves are wetted immediately after the deposi tion of conidia. Apparently, conidia do not readily germinate in a free-moisture film. A striking illustration of the influence of water is the fact that during the late 1930s and early 1940s, when spider mites on roses were controlled by frequent water sprays, powdery mildew was rarely a problem, although black spot was very serious. Since the late 1940s, miticide (acaricide) sprays and aerosols have replaced this procedure; black spot has essentially disappeared in greenhouse roses, but powdery mildew is again quite serious. In the field, the most favorable conditions for powdery mil dew are as follows. At night, a temperature of 15.5°C and a rela tive humidity of 90–99% allow optimal conidium formation, conidium germination, and infection. Conditions of 26.7°C and 40–70% relative humidity during the day favor the maturation and release of conidia. Several repeated night–day cycles of these conditions are necessary for an epidemic to develop.

Management New rose cultivars continue to be produced, and many show resistance to powdery mildew. However, few retain a high level of resistance, presumably because of the development of new races of P. pannosa that can overcome this resistance. Control has mainly been achieved using protective fungicidal sprays. Since the early 1980s, interest has been increasing in the use of systemic fungicides and in reduced-risk fungicides. Control measures for outdoor and greenhouse roses differ somewhat. On outdoor roses, powdery mildew can be expected to occur when rainfall is low or absent, the temperature range is near optimal, and the humidity is high at night and low dur ing the day. Should these conditions occur, the use of protective fungicidal sprays is warranted. The rapid production of suscep tible shoots necessitates repeated application, and the timing of applications is extremely important. Pruning infected shoots at the end of the season and destroying these shoots in regions where winters are severe help prevent overwintering of the fungus. Raking and destroying fallen leaves from around rose bushes at the end of the season may also inhibit overwintering. On greenhouse roses, powdery mildew can be expected to occur when the temperature range is near optimal and the hu midity is high at night and low during the day. When these conditions exist, the occurrence of powdery mildew may be 8

forecast 3–6 days before it appears. Thus, protective fungicidal sprays should be applied and repeated on a 7-day schedule as long as these conditions persist. Other preventive control mea sures include lowering the night humidity by using fans, vent ing, or both or by heating and venting. Selected References Bender, C. L. 1982. Pathogenic specialization and heterothallism in Sphaerotheca pannosa var. rosae. Ph.D. thesis. Oregon State Uni versity, Corvallis, OR. Bender, C. L., and Coyier, D. L. 1982. Identification of five races of Sphaerotheca pannosa var. rosae. (Abstr.) Phytopathology 72:983. Braun, U. 1995. The powdery mildews (Erysiphales) of Europe. Gustav Fischer Verlag, Jena, Germany. Coyier, D. L. 1961. Biology and control of rose powdery mildew. Ph.D. thesis. University of Wisconsin, Madison. Dimock, A. W., Tammen, J., Nichols, L., and Nelson, P. E. 1987. Powdery mildew of roses. Pages 289-296 in: Roses: A Manual of Greenhouse Rose Production. R. W. Langhans, ed. Roses Inc., Has lett, MI. Horst, R. K. 2001. Color plate 5A in: Westcott’s Plant Disease Hand book, 6th ed. Revised by R. K. Horst. Kluwer Academic Publishers, Boston. Kunoh, H. 1995. Host-parasite specificity in powdery mildews. Pages 239-250 in: Pathogenesis and Host Specificity in Plant Diseases: Histopathology, Biochemistry, Genetics, and Molecular Bases, Vol. 2, Eukaryotes. K. Kohmoto, U. S. Singh, and R. P. Singh, eds. Per gamon Press (Elsevier), Oxford. Linde, M., and Shishkoff, N. 2003. Fungi: Powdery mildew. Pages 158-165 in: Encyclopedia of Rose Science, Vol. 1. A. Roberts, T. Debener, and S. Gudin, eds. Academic Press (Elsevier), Oxford. Pady, S. M. 1972. Spore release in powdery mildews. Phytopathology 62:1099-1100. Perera, R. G., and Wheeler, B. E. J. 1975. Effect of water droplets on the development of Sphaerotheca pannosa on rose leaves. Trans. Br. Mycol. Soc. 64:313-319. Salmon, E. S. 1900. A monograph of the Erysiphaceae. Mem. Torrey Bot. Club 9. Wheeler, B. E. J. 1978. Powdery mildews of ornamentals. Pages 411-4 45 in: The Powdery Mildews. D. M. Spencer, ed. Academic Press, London. Woronichine, N. 1914. Quelques remarques sur le champignon du blanc de pecher. Bull. Soc. Mycol. Fr. 30:391-401.

Black Spot Black spot has also been called leaf blotch, leaf spot, blotch, rose Actinonema, rose leaf Asteroma, and star sooty mold. It is the most important disease of roses all over the world. Black spot is a minor problem on greenhouse roses, because greater care is taken to avoid syringing plants with water for spider mite control and because humidity is regulated very carefully. On outdoor roses, however, this disease is generally present, frequently epidemic, and a major problem. Black spot is widespread in Europe. It was first reported in Sweden in 1815 and was reported in France, Belgium, Ger many, England, and the Netherlands by 1844. The disease is found throughout the United States. It was first recorded in the northeastern United States in 1830. Black spot was reported in South America in 1880, Australia in 1892, the Soviet Union in 1907, China in 1910, Canada in 1911, Japan in 1914, Africa in 1920–1922, India in 1941, and Turkey in 1947. The pathogen has been widely distributed with cultivated roses and is now found even in oceanic islands, such as the Philippines, Malta, Hawaii, and New Zealand.

Symptoms Characteristic black spots 2–12 mm in diameter develop on upper leaf surfaces. These leaf spots are circular or irregu

larly coalescent with characteristic feathery, radiate, fibrillose margins of subcuticular mycelial strands (Fig. 10). In some in stances, the feathery lesion margin may be indistinct. Small black acervuli are often visible on the surface (Figs. 11 and 12) and may be distributed irregularly or in concentric circles. Conidia may be visible as white, slimy masses on the acervuli. Leaf tissue surrounding the spots turns yellow, and chlorosis extends throughout the leaflet until abscission occurs. The pathogen is actually present only in the lesion itself; the yellow tissue is caused by pathogen metabolites. The yellow tissue ex hibits a high level of metabolic activity that is expressed by the accumulation of phenolics and ortho-dihydroxyphenols and amino acids, as well as by a high level of enzymatic activity. Spots enlarge slowly, taking several weeks to reach 12 mm in

diameter. In resistant cultivars or under unfavorable environ mental conditions, only tiny, black flecks may form and leaves may not turn yellow or abscise. Yellowing (Fig. 13) and abscission of leaflets are associated with ethylene. Leaves with black spot produce large amounts of ethylene; production decreases as leaves become yellow and ceases when leaves turn brown. Infected leaves con tain less auxin than do healthy ones. The pathogen degrades this abscission-retarding material, thereby hastening leaf abscission. Raised, purple-red, irregular blotches develop on the im mature wood of first-year canes of susceptible cultivars (Fig. 14). Spots later become blackened and blistered; they contain acer vuli but lack fibrillose strands. Lesions are often small and rarely kill branches but are extremely important in the survival of the pathogen over the winter. Petioles and stipules may have inconspicuous black spots similar to those found on leaves. Petioles may be girdled with out abscising. Peduncles, fruits, and sepals may have similar symptoms. Petals may have red flecks accompanied by moder ate distortion. Acervuli frequently occur in the lesions.

Causal Organism

Marssonina rosae (Asteroma rosae Lib., Actinonema rosae (Lib.) Fr., and Marssonia rosae Trail), the anamorph stage of the black spot pathogen, was described in France in 1827. The teleomorph stage, Diplocarpon rosae, was described in New York in 1912. The pathogen is quite host specific and ap proaches obligate parasitism. Pathogenic races of the fungus are reported.

Fig. 10. Early lesions on a leaf affected by black spot, caused by Diplocarpon rosae.

Fig. 12. A close-up of acervuli of Diplocarpon rosae, the cause of black spot, in a lesion on a leaf.

Fig. 11. Acervuli of Diplocarpon rosae, the cause of black spot, in a lesion with feathery margins.

Fig. 13. Severe symptoms of black spot, caused by Diplocarpon rosae. Note the lesions with yellowing from the formation of ethylene.

Parasitic mycelia of M. rosae are characteristically sub cuticular, radiate, branching, and single or in strands of paral lel hyphae. Hyphae are hyaline when young, but they darken with age. Haustoria are formed in host cells. Acervuli are sub cuticular and irregularly rupture the cuticle. Acervuli vary in diameter from 50 to 400 µm. Each acervulus bears two-celled, hyaline conidia (Fig. 15B). The conidia (5–7 × 15–25 µm) are smooth with a sticky surface and occur in a white, slimy mass. Dead leaf tissues contain intercellular and intracellular my celia and lack haustoria. Apothecia are rarely formed; they have been reported twice from the northern United States and Canada (in the period from October to December) and twice from England (in the period from April to May). Apothecia measure 100–250 µm in diameter and have a circular, sub cuticular shield of dark brown, thick-walled cells. Asci (15 × 70–80 µm) contain eight hyaline ascospores (5–6 × 20–25 µm). Ascospores are forcibly discharged and are airborne; they are not water-dispersed. The fungus grows on potato dextrose or malt agar but re quires 15–37 days to form a visible colony from a single spore and 1 month to reach a colony diameter of 2–9 mm. Virulence may be lost in a few months in culture.

Disease Cycle

Leaves are most susceptible while still expanding (6–14 days old). Both upper and lower leaf surfaces are susceptible. To germinate, conidia must be wetted at least 5 min even if held at 100% humidity. Regardless of the relative humidity, conidia must be immersed in water and must be continuously wet for at least 7 h for any infections to occur. A conidium germinates in 9–18 h on a moist leaf at 22–26°C. Germ tubes emerge from the larger cell of the conidium and infrequently from both cells. Germ tubes penetrate the leaf cuticle and grow between the cu ticle and epidermal cells. Fine hyphae branch vertically, pene trate the epidermal cell wall, expand into the bulbous structure outside the plasmalemma, and produce haustoria. Haustoria may form within host cells 15 h after infection. Secondary mycelium forms on the second day, and in 3–5 days, parallel, subcuticular strands are formed. By the sixth and seventh days, there may be as many as five to eight haustoria per cell. Infections on lower leaf surfaces resemble those on upper surfaces, except that hyphae soon grow through the mesophyll,

developing on both upper and lower surfaces. Symptoms ap pear in 3–16 days, depending on temperature and inoculum. Acervuli form in 11 days on the upper leaf surface and in 1 month on the lower leaf surface. When the relative humidity decreases at the location of the enlarging acervulus, the cu ticle breaks, exposing a slimy mass of conidia. Conidia may be produced 10–18 days after infection. Production of conidia by a given acervulus decreases after about 1 week and may end after 10 days, but new acervuli are continually formed at the margins of the spots. Some conidia adhere to ruptured cuticle fragments, but most are dispersed in rainwater or condensate. Conidia are dissemi nated by splashing water, by people during cultivation, or by contact with sticky body parts of insects. Fallen leaves blown by the wind may disperse the pathogen locally, but conidia are usually airborne only in water drops. Ascospores are found so rarely that they are unimportant in dispersal. Infected plants may introduce the fungus into greenhouses. The fungus does not survive in the soil, and conidia adhering to tools, benches, etc., remain viable no longer than 1 month. In areas with mild climates and in greenhouses, the fungus remains active on the host throughout the year. The fungus overwinters in several ways: as mycelia in fallen leaves or in in fected canes that may produce either new acervuli or apothecia in which conidia and ascospores form each spring (Fig. 15A); as conidia in existing acervuli in fallen leaves; or as acervuli in which new conidia are produced in the spring (Fig. 15C).

Epidemiology M. rosae tolerates a wide range of temperatures (15–27°C), mainly through an inverse relation of humidity and moisture. Conidium germination is optimal at 18°C; at this temperature, germination begins in 9 h and may reach 96% in 36 h. The pathogen is sensitive to high temperatures. Conidia are killed without germinating at 33°C; whereas at 30°C, they may ger minate but fail to develop further. Mycelial growth is optimal at 21°C and is halted after 8 weeks at 33°C. Conidial infection of leaves is optimal at 19–21°C, and symp toms may develop within 3–4 days at 22–30°C. Disease devel opment is optimal at 24°C. No infections occur if leaf surfaces are dried within 7 h of inoculation and incubated at 15–24°C. The likelihood of infection increases if leaves remain moist for 24 h before drying. No infection occurs in dry air. Even at 100% relative humidity, no germination occurs if conidia have not been wetted, and at a relative humidity below 90%, mature conidia must be immersed in water for at least 7 h before they can cause infection. Conidia begin to germinate as early as 8 h after being wetted. Good air circulation around roses in greenhouses or in the field hastens drying and reduces the likelihood of black spot. However, cool, moist ocean winds in coastal regions or over head irrigation favors infection. Disease development is re stricted in arid regions or in greenhouses with low humidity where irrigated plants dry rapidly. Summer heat and winter cold limit the development of epidemics in rainy regions.

Management

Fig. 14. Canes infected with the black spot fungus, Diplocarpon rosae.

Leaves should not be allowed to remain wet or at a very high humidity for more than 7–12 h. Plants should not be syringed with water; if syringing is practiced, it should be done only on bright mornings with rising temperatures. Excessive watering should be avoided during dark, humid weather. Overhead wa tering of landscape roses should be avoided, but if practiced, watering should occur in the early morning to allow the foliage ample time to dry throughout the day. Removing leaves from the ground and pruning canes that contain lesions inhibit overwintering of the pathogen. Dense plantings should be avoided to allow good air circulation through the leaf canopy.

Fungicidal sprays should be applied during periods of the year when conditions are favorable for black spot develop ment. In the northeastern United States, preventive fungi cidal sprays should be initiated around budbreak and should continue bimonthly until leaf emergence on landscape roses. Thereafter, fungicides should be applied every 7 days. Good control can be obtained with fungicidal sprays every 14 days if surfactants are used in sprays with wettable powder fungicides. Black spot resistance in roses is rare, especially in tetraploid roses. Cultivars reported to be highly resistant are the “Knock Out” series; Alba Meidiland; All That Jazz; Baby Love; Belinda’s Dream; Caldwell Pink; the “Griffith Buck” series, such as Carefree Beauty, Carefree Delight, Carefree Sunshine, Carefree Wonder, Prairie Sunrise, Prairie Harvest, and Distant Drums; the Canadian “Explorer” series, such as Simon Fraser, John Davis, William Baffin, Champlain, Henry Kelsey, and Charles Albanel; named rugosa cultivars, such as Blanc Double

de Coubert, Hansa, Therese Bugnet, Marie Bugnet, and Frau Dagmar Hastrup (Frau Dagmar Hartopp); and the “Pavement” series, such as Purple Pavement, Snowy Pavement, and Pink Pavement. The occurrence of pathogenic races of the fungus makes it difficult to develop resistant cultivars. In general, teas, hybrid teas, hybrid perpetuals, pernetianas, Austrian bri ers, and polyanthas are quite susceptible and hybrid rugosas, moss roses, and wichuraianas are more resistant. Durable black spot resistance has been reported in the antique rose cultivars Blanc Double de Coubert, Frau Dagmar Hastrup, Konigin von Danemark, and Maiden’s Blush. Among rootstocks, the ‘Welch’ and ‘Tate’ strains of Rosa multiflora Thunb. ex Murray are highly resistant, and R. odorata (Andrews) Sweet, R. ma netti Bals.-Criv. ex Rivers, R. caudata Baker, ‘IXL’, ‘Texas Wax’, and ‘Ragged Robin’ are susceptible; however, it has been reported that disease susceptibility is a characteristic of the scion, and understocks are not known to influence the disease susceptibility of the scion.

Fig. 15. Black spot disease cycle. A, Diplocarpon rosae overwinters in infected canes or buds and in fallen leaves. B, New shoots are infected from overwintering mycelium or from water-splashed conidia or airborne ascospores produced on fallen leaves, sometimes in the same lesion. C, Leaves and canes are infected during the summer by airborne ascospores or by water-splashed conidia produced on infected leaves.

Selected References Aronescu, A. 1934. Diplocarpon rosae: From spore germination to haustorium formation. Bull. Torrey Bot. Club 61:291-329. Baker, K. F., and Dimock, A. W. 1987. Black spot. Pages 297-309 in: Roses: A Manual of Greenhouse Rose Production. R. W. Langhans, ed. Roses Inc., Haslett, MI. Bhaskaran, R., Purushothaman, D., and Ranganathan, K. 1974. Physio logical changes in rose leaves infected by Diplocarpon rosae. Phy topathol. Z. 79:231-236. Bolton, A. T., and Svejda, F. J. 1979. A new race of Diplocarpon rosae capable of causing severe black spot on Rosa rugosa hybrids. Can. Plant Dis. Surv. 59:38-40. Castledine, P., and Roberts, A. V. 1981. Cuticular resistance to Diplo carpon rosae blackspot fungus disease of roses. Trans. Br. Mycol. Soc. 77:665-666. Cook, R. T. A. 1981. Overwintering of Diplocarpon rosae at Wisley, England. Trans. Br. Mycol. Soc. 77:549-556. Debener, T., Drewes-Alvarez, R., and Rockstroh, K. 1998. Identifi cation of five physiological races of blackspot (Diplocarpon rosae Wolf) on roses. Plant Breed. 117:267-270. Drewes-Alvarez, R. 2003. Fungi: Blackspot. Pages 148-154 in: En cyclopedia of Rose Science, Vol. 1. A. Roberts, T. Debener, and S. Gudin, eds. Academic Press (Elsevier), Oxford. Knight, C., and Wheeler, B. E. J. 1977. The germination of Diplocar pon rosae on different rose cultivars. Phytopathol. Z. 91:346-354. Morrison, L. S., and Russell, C. C. 1976. Timing of fungicide–adjuvant mixtures for control of rose blackspot. Plant Dis. Rep. 60:634-636. Palmer, J. G., Sachs, I. B., and Semeniuk, P. 1978. The leaf spot caused by Marssonina rosae observed in scanning electron microscopy and light microscopy. Scanning Electron Microsc. 2:1019-1026. Singh, S. N. 1980. Effect of rootstock on growth, flowering and dis ease resistance of hybrid tea roses. Prog. Hortic. 12(3):5-14. Sohi, H. S., and Prakash, O. M. 1974. Reaction of rose varieties against blackspot, Diplocarpon rosae, disease. Indian Phytopathol. 27:119-120. Svejda, F. 1979. David Thompson rose, Rosa rugosa. Can. J. Plant Sci. 59:1167-1168. Svejda, F., and Bolton, A. T. 1980. Resistance of rose hybrids to three races of Diplocarpon rosae. Can. J. Plant Pathol. 2:23-25.

In England, P. mucronatum, P. tuberculatum, P. fusiforme, and P. rosae-pimpinellifoliae have been found on more than 200 named cultivars of bush roses (hybrid teas and floribundas); P. tuberculatum is the most common (Table 1). P. mucrona tum and P. tuberculatum are now considered to be conspecific or variants of the same species. Additional conspecificity may be found with taxonomic reevaluation using molecular taxon omy. Although rust on roses is generally widespread, it is more common in southern and eastern England, the western United States, and other geographic areas where low temperatures and high moisture levels during certain times of the year are condu cive for disease development.

Symptoms

The disease first appears on leaves and other green parts of the plant as powdery pustules of orange aeciospores, usu ally confined to lower leaf surfaces (Figs. 16 and 17). In early spring, spore masses may be inconspicuous and go unnoticed. As pustules develop, they become visible on upper leaf surfaces as orange or brown spots (Fig. 18). Young stems and sepals may also become infected (Fig. 19) and finally distorted.

Rust Nine species of the rust fungus genus Phragmidium are found on roses: P. mucronatum, P. tuberculatum, P. fusiforme, P. rosae-pimpinellifoliae, P. americanum, P. montivagum, P. rosae-californicae, P. rosicola, and P. speciosum. All of these species have been reported on native species of roses, and P. mucronatum, P. americanum, P. fusiforme, P. speciosum, and P. tuberculatum may occur on cultivated roses as well. P. mucronatum is the most common rust species in the United States on hybrid teas and on other roses with large, firm leaflets.

Fig. 16. Orange pustules of the uredial stage of the rust fungus Phragmidium mucronatum on lower leaf surfaces. (Reprinted, by per mission, from Horst, 2001)

Cultivars vary widely in susceptibility and reaction to in fection. Leaves of some cultivars may become covered with pustules and yet remain attached to the plant, while a single rust pustule on a leaflet of another cultivar causes the leaflet to fall. Susceptible and moderately susceptible cultivars are Ar lene Francis, Aztec, Baby Blaze, Betsy McCall, Blue Moon, Buccaneer, Christopher Stone, Chrysler Imperial, Circus, Confidence, Dearest, Elizabeth of Glamis, Embers, Fragrant Cloud, Fusilier, Golden Girl, Golden Masterpiece, Heat Wave, Helen Traubel, Jeanie, Josephine Bruce, Kordes Perfecta, Mon tezuma, New Yorker, Nocturne, Peace, Piccadilly, Pink Peace, Pink Radiance, Queen Elizabeth, Siren, Spartan, Sutter’s Gold, Talisman, The Doctor, Virgo, Vogue, Wendy Cussons, White Bouquet, White Knight, and White Swan. Many other cultivars not included on this list are also susceptible. The summer uredial stage has reddish orange pustules and may repeat every 10–14 days under favorable environmental conditions. The repeating summer uredial stage is followed by the wilting and defoliation of susceptible cultivars. In mild cli

Fig. 17. A close-up of the uredial stage of the rust fungus Phragmidium mucronatum on a lower leaf surface. (Reprinted, by permis sion, from Horst, 2001)

Fig. 18. Chlorotic spots of rust, caused by Phragmidium mucrona tum, on upper leaf surfaces. (Courtesy K. Ohkawa)

mates, the uredial stage continues; in cooler areas, black, telialstage pustules are formed toward autumn (Fig. 20).

Causal Organisms

P. mucronatum and P. tuberculatum are the two species of the genus Phragmidium most commonly found to cause rust on cultivated roses. P. mucronatum was the first fungal parasite to be seen with a microscope in 1665 by Hooke, who gave a careful drawing, complete with scale, of the teliospore on a rose leaf. Rust fungi with a complete life cycle have five different spore forms, which are numbered 0–IV: 0, spermatia formed in sper magonia; I, aeciospores in aecia; II, urediospores in uredinia; III, teliospores in telia; and IV, basidiospores on basidia. In heteroecious rusts, spore stages 0 and I are formed on one host and stages II and III on another. Stage IV always follows stage III after germination. Although most autoecious rusts have all spore forms on one host, a few short-c ycle rusts fail to pro duce all spore stages. There are no known alternate hosts for rose rust. The nine species of the genus Phragmidium that cause rust on roses, the spore stages found on roses, and the number of

Fig. 19. The uredial stage of the rust fungus Phragmidium mucronatum on a cane.

Fig. 20. Black pustules of the telial stage and orange pustules of the uredial stage of the rust fungus Phragmidium mucronatum on leaf surfaces. (Courtesy V. A. Wager)

cells in the teliospores used for species determination (Fig. 21) are found in Table 1. Axenic cultures of P. mucronatum can be grown success fully on agar media containing yeast extract, peptone, and ca sein hydrolysate thickly seeded with urediospores.

Epidemiology Spores from rust pustules are air-transmitted and infect rose leaves through stomatal openings. The optimal temperatures for development of the disease are 18–21°C, and continuous moisture for 2–4 h is essential for the establishment of infec tion. On susceptible cultivars in greenhouses, infection is likely to be severe near ventilators where condensation occurs. Teliospores have a stalked pedicel, which has a swelling in the lower portion (Fig. 21). A gelatinized wall forms at the base of the teliospore and may fix the spore in a position suitable for producing basidia in the spring. In late summer and early autumn, black pustules appear on outdoor-grown roses, often in the same affected leaf areas in which teliospores are found (Fig. 22). Black pustules over winter within the leaf and stem tissues (Fig. 23) after the leaves

fall, and they later produce spores for spring infections. In areas with severe winters, the rust fungus may not overwinter, and the summers are usually dry enough that there is little in crease in the the likelihood of the rust disease. High summer temperatures inhibit infection; urediospores retain viability for only 1 week at 27°C.

Management Removing infected leaves during the season and all old leaves left at the time of winter or early spring pruning before new leaves appear helps to reduce inoculum levels and prevents the early appearance of disease. Spring pruning of old canes helps to eliminate rust carryover on canes. Any means of preventing condensation in greenhouses aids in controlling rust since free moisture for several hours is es sential for infection. Preventive fungicidal sprays should be applied every 7 days during periods when environmental conditions favor disease development. Selected References

Fig. 21. Teliospores of Phragmidium mucronatum, the cause of rust. (Courtesy K. Milne)

Anthony, V. M., Shattock, R. C., and Williamson, B. 1985. Interaction of red raspberry cultivars with isolates of Phragmidium rubi-idaei. Plant Pathol. 34:521-527. Bhatti, M. H. R., and Shattock, R. C. 1980. Axenic culture of Phrag midium mucronatum. Trans. Br. Mycol. Soc. 74:595-600. Horst, R. K. 2001. Phragmidium. Pages 430-432 in: Westcott’s Plant Disease Handbook, 6th ed. Revised by R. K. Horst. Kluwer Aca demic Publishers, Boston. Howden, J. C. W., and Jacobs, L. 1973. Report on the rust work at Bath. Rose Annu. (R. Natl. Rose Soc.) 1973:113-119. Ingold, C. T., Davey, R. A., and Wakley, G. 1981. The teliospore pedicel of Phragmidium mucronatum. Trans. Br. Mycol. Soc. 77:439-4 42. Nichols, L. P., and Nelson, P. E. 1987. Foliage diseases. Pages 311320 in: Roses: A Manual of Greenhouse Rose Production. R. W. Langhans, ed. Roses Inc., Haslett, MI. Shattock, R. C. 2003. Fungi: Rust. Pages 165-169 in: Encyclopedia of Rose Science, Vol. 1. A. Roberts, T. Debener, and S. Gudin, eds. Academic Press (Elsevier), Oxford.

Fig. 22. The telial stage and the uredial stage of the rust fungus Phragmidium mucronatum on the same leaf. (Courtesy K. Milne)

Fig. 23. The overwintering telial stage of the rust fungus Phragmidium mucronatum on canes.