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Huanglongbing in China: a Historical

Perspective

South China Agricultural University

Yijing Cen

Department of Entomology

Citrus Huanglongbing Research Laboratory

South China Agricultural University

E-mail: cenyj@scau.edu.cn

1. History of HLB in China

2. Current distribution and status of HLB in China

3. Control of HLB in China

4. Current research in HLB control

Outline

Fruit production in China

Kiwi

0.5%

Jujube

2.9%

Persimmon

2.4%

Others

9.8%

Longan

1.1%

Banana

7.4%

Grape

6.4%

Lychee

1.6%

Peach

8.6%

Pineapple

0.9%

Citrus

19.6%

Pear

12.3%

Apple

26.5%

Totalyield

105.2MillionTons

(http://citrus948.hzau.edu.cn)

Citrus Varieties in China

Tangerine

37.3%

Mandarine

33.4%

Others

1.3%Pummelo

11.0%

Orange

17.0%

Huanglongbing is the most destructive citrus disease in China

The trees decline and lose their economic value once infected

Taken by Xiaoling Deng

Tree decline due to HLB infection

First report of

HLB in

Chaoshan,

Guangdong

Province, China

(Reiking, 1919)

1. History of HLB in China

A report of HLB in Guangdong in 1923

Journal of Lingnan

Agricultural University

Symptom: Yellow

chicken head

For control, prune it

off

Lingnan Agricultural University:

predecessor of South China

Agricultural University (SCAU)

HLB infected citrus trees in Chaoshan in 1930’S

A dispute persisted over the cause of HLB

between Horticulturists and Plant

Pathologists for over 30 years.

Horticulturists: suggested it was caused by

nutritional deficiencies

Plant Pathologists: suggested it was

caused by pathogen of plant disease

Prof. Lin Kongxiang

(1910-1985)

1 Observations of citrus yellow shoot (huanglong)

disease. Acta Phytopathol. Sinica. 1956a, 2: 1-11.

2 Etiological studies of citrus yellow shoot (huanglong)

disease. Acta Phytopathol. Sinica. 1956b, 2: 13-42.

The dispute persisted until prof. Lin from South China Agricultural University published his 2 papers demonstrating that it was an infectious disease in 1956.

Report of ACP in China:

Taiwan Island in 1908 (Kuwayama, 1908); Macau in 1927 (Husain & Nath, 1927)

First record in mainland China in 1936 (Hoffmann et al. 1936. Journal of Lingnan

Agriculture, 2(1):202-205)

First found on

wampee and

citrus in Lingnan

University

campus

(Guangzhou) in

Nov.1934.

The host plants of Asian citrus psyllid in China

• Murraya

• Citrus

• wampee

Clausena lansium

wampee Murraya exotica

Little attention was paid to ACP until

1953, Prof. Huang Bangkan from

Fujian Agriculture and Forestry College

reported that it was important pest of

citrus young shoots and published

results of his biological studies.

adults

Vector of HLB-Asian citrus psyllid (ACP)

ACP was proved to

be the vector of HLB

in 1976 by:

Guangdong HLB

Research Team and

Guangxi HLB

Research Team

simultaneously.

New vector of HLB found in Yunnan Province,

China: Pomelo psyllid Cacopsylla (Psylla)

citrisuga Yang & Li (Cen et al. 2012)

Adult nymphs Damage phenotype

The history of HLB in Guangdong Overseas Chinese

Citrus Farm reflects the history of HLB in China.

A state-run farm, 2000ha citrus, used to be:

• the most important citrus farm in China

Citrus was first successfully planted up in the mountanious region.

HLB control experience was first developed from this farm

• the biggest citrus farm in Asia

1. History of HLB in China

The history of HLB in Guangdong Overseas Chinese

Citrus Farm

• Before 1976, main citrus pests were big defoliating

insects. Although ACP had not been proven to be the

vector of HLB, it had been very well controlled by

broad-spectrum insecticides while controlling other

pests;

• After 1976, the secondary, small sap-feeding pests,

especially citrus red mites became major pests.

Acaricides use resulted in high populations of ACP

and high infection of HLB. All citrus were removed.

1. History of HLB in China

The history of HLB in Guangdong Overseas Chinese

Citrus Farm

1980-1994 New plantings were assigned as small

plots to workers. However, all agricultural means of

production were provided by the state. ACP and HLB

were under good control, below 0.1% HLB infection

every year.

After 1994 The state stopped investing and all citrus

trees were sold to the workers. Poor ACP control and

nutrition resulted in very high and early HLB

infection in many plots.

1. History of HLB in China

HLB and ACP are now widely distributed in 11 of the 18 citrus plantation

provinces: Guangdong, Guangxi, Fujian, Hainan, Taiwan, Jiangxi, Zhejiang,

Guizhou, Yunnan, Hunan, and south part of Sichuan.

2. Current distribution and status of HLB in

China

Severely infected

Partly infected

Pummelo

Jiaogan

mandarine

Nianju

tangerine

Shatangju

tangerine

Gonggan

mandarine

Mashuiju

tangerine

Hongjiang

orange

Shatangju

tangerine

Chuntianju

tangerine

Wenzhou mandarin,

pummelo

Xinhuigan mandarine Citrus cultivars in Guangdong Province:

Most are mandarine and tangerine,

very susceptible to HLB.

Huazhou

tangerine

ShatangjuTangerine:

The most popular and

famous cultivar in

Guangdong

Very tasty and fertility

ShatangjuTangerine

Infected with HLB

Taken by

Xiaoling Deng

Citrus production in China

(http://citrus948.hzau.edu.cn)

Although greatly impacted by HLB, citrus production has been increasing in

China since 1980s. Up to 2009, total citrus acreage was 2 million ha., total yield

was 25 million tons. Since 2010, about 2.2million ha., 27 million tons per year.

One objective: to develop citrus in areas

where HLB and ACP are absent

.

Mandarin orchard in Hubei Province

Taken by

Xiaoling Deng

Lemon orchards in Yunnan Province

(southwest)

Taken by

Xiaoling Deng

Jiaogan

Chaozhou, Guangdong

High density plantation in HLB present area: about 1000 trees/ha.

In regions where HLB is present, the key

management strategies are:

HLB-free nursery stocks

Sanitation of the planting environment

Improvement of tolerance in uninfected trees

Removal of infected trees when the infection rate

is still low

Insect vector (Asian citrus psyllid) management

3. Control of HLB in China

3.1 Planting HLB-free nursery stocks

Modern, standard disease-free nursery in Hunan

Simple disease-free nursery in Guangxi and Guangdong

1ha per shed

Bad nursery in Guangdong

Bad nursery in Guangdong

HLB infected young citrus trees in Guangdong

Taken by

Xiaoling Deng

Experience from some farmers in Guangdong: planting the 2 or 3

year-old young plants to reduce the risk of HLB infection. Trees are

expected to get fruits 1 year after planted.

3.2 Sanitation of the planting environment

Ganzhou, Jiangxi Province (navel orange)

Taken by

Xiaoling Deng

Infected old grove

In China, successful development

of young plants beside infected

orchards is not possible.

3 years 1 year

2 years

Unfortunately, some farmers do not understand……

Picture from Xiaoling Deng

HLB was not transmitted by the

infected trees to healthy citrus when

they were planted directly together

even after 3 years.

Possibility of the root transmission of HLB

36.67% healthy plants became

infected 1 year after root grafting

with the infected plants.

Xu et al, 2015

3.3 Improvement of the plant tolerance

A healthy Jiaogan (Chaozhou Gan) orchard in Chaozhou, where HLB was

first reported. The owner, Mr. Lai said he only used organic fertilizers,

never used chemical fertilizers. Insecticides were applied only for

dormancy spray.

Applying organic fertilizers is long believed to

improve citrus tolerance to HLB and ACP.

Photo of the owner of the healthy Jiaogan orchard, Mr.

Lai (left) and Mr. Jiacheng Li (right, the Richest

Chinese) .

3.4 Eradication of infected citrus trees

• The only official recommendation in China: eradication of infected trees

• Annual surveys are undertaken during October-December when symptoms are showing up most remarkably.

The only recommended way

in China: eradication of

infected trees

Infected tree stump

lack of agricultural machinery

Treated

method of the

infected

stumps

1 2

3 4

5 Picture from Xianjin Bai

ACP control: Cultural and Chemical control

Cultural control

•Applying of organic fertilizers

•Planting windbreak trees around the orchard

•Control of the new flushes

•Elimination of the infected trees as soon as

they are recognized, because they are more

attractive to ACP.

3.5 Management of the vector-

Asian citrus psyllids

Chemical control

Insecticides are used:

• for dormancy (sanitation) spray after harvest.

• during sprouting. 1-2 sprays for 1 sprouting season.

• before infected trees being eliminated.

Chemical insecticides (such as imidacloprid,

organophosphorus and pyrethroids) are commonly

mixed with 0.5% mineral spray oil to get better

effect and longer term of protection.

ACP adults were

found on the trunk

soon after

insecticides used

Spray result Aerosol sprayer

• Aerosol spray is recommended in Guangxi.

• Cost: 225 Yuan ($36) /ha. Including pesticides and labour.

• More complete control

• Depends on circumstance and weather

Picture from Xianjin Bai

4 Current research in HLB control

1. Antibiotics

Tetracycline was reported to be most effective on HLB in

1970s and has been recommended for elimination of

infection in scions and seeds of rootstock.

2. Heat treatment

3. Nutrition program

Nutritional programs aimed at infected trees have not been

as effective as reported from Florida.

Possible reason: different varieties? soil?

4. Vector control:

Improvement of yellow sticky traps; biological control

In summary

HLB:

1. No solution to the pathogen currently

Candidatus Liberibacter spp.: uncultured, limited in

the phloem of the host plants

2. Can be prevented by the “5 strategies”

Murraya exotica

Future solution aims at the

pathogen: GMO?

Murraya exotica: immune to HLB

Acknowledgement

Elizabeth Baldwin, USDA-ARS Horticultural Research

Laboratory

Philip A. Stansly, James A. Tansey, UF/IFAS/SWFREC

Andrew Beattie, University of Western Sydney

Jianchi Chen, USDA-ARS San Joaquin Valley

Agricultural Sciences Center

Yulu Xia, North Carolina State University

Xiaoling Deng, Changbao Xu, Meirong Xu, and all

students from Citrus Huanglongbing Research

Laboratory, SCAU

Ministry of Agriculture of China

Chinese Scholarship Council

South China Agricultural University

Thank you

for your

attention!

Yijing Cen岑伊静

cenyj@scau.edu.cn

cenyj@ufl.edu

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