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South Agricultural University

Huanglongbing in China: a Historical Perspective

Yijing Cen

Department of Entomology Citrus Huanglongbing Research Laboratory South China Agricultural University

E-mail: [email protected] Outline

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

Fruit production in China

Longan Lychee 1.1% 1.6% Pineapple 0.9% Peach 8.6%

Banana Kiwi 7.4% 0.5% Grape 6.4% Citrus Jujube 19.6% 2.9% Total yield Persimmon 105.2Million Tons 2.4% Pear 12.3% Others 9.8%

Apple 26.5% (http://citrus948.hzau.edu.cn) Citrus Varieties in China

Others Pummelo 1.3% 11.0% Mandarine 33.4% Orange 17.0%

Tangerine 37.3% Taken by Xiaoling Deng

Huanglongbing is the most destructive citrus disease in China The trees decline and lose their economic value once infected Tree decline due to HLB infection 1. History of HLB in China

First report of HLB in , Province, China (Reiking, 1919) A report of HLB in Guangdong in 1923 For control, prune it off

Journal of Agricultural University

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

Prof. Lin Kongxiang 1 Observations of citrus yellow shoot (huanglong) (1910-1985) disease. Acta Phytopathol. Sinica. 1956a, 2: 1-11.

2 Etiological studies of citrus yellow shoot (huanglong) disease. Acta Phytopathol. Sinica. 1956b, 2: 13-42.

First found on wampee and citrus in Lingnan University campus () in Nov.1934.

Report of ACP in China: 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)

The host plants of Asian citrus psyllid in China

• Murraya • Citrus • wampee Clausena lansium

wampee Murraya exotica Vector of HLB-Asian citrus psyllid (ACP)

Little attention was paid to ACP until 1953, Prof. Huang Bangkan from Agriculture and Forestry College reported that it was important pest of citrus young shoots and published results of his biological studies.

adults ACP was proved to be the vector of HLB in 1976 by: Guangdong HLB Research Team and HLB Research Team simultaneously. Adult nymphs Damage phenotype

New vector of HLB found in Province, China: Pomelo psyllid Cacopsylla (Psylla) citrisuga Yang & Li (Cen et al. 2012) 1. History of HLB in China 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.

2. Current distribution and status of HLB in China

Severely infected

Partly infected

HLB and ACP are now widely distributed in 11 of the 18 citrus plantation provinces: Guangdong, Guangxi, Fujian, Hainan, Taiwan, Jiangxi, , , Yunnan, Hunan, and south part of Sichuan. mandarin, pummelo Pummelo Nianju Shatangju tangerine tangerine

Shatangju tangerine

Gonggan mandarine

Mashuiju tangerine Huazhou tangerine Chuntianju Jiaogan tangerine mandarine

Xinhuigan Hongjiang mandarine Citrus cultivars in Guangdong Province: orange Most are mandarine and tangerine, very susceptible to HLB.

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 , Guangdong

High density plantation in HLB present area: about 1000 trees/ha. 3. Control of HLB in China

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

 3.1 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 Taken by Xiaoling Deng HLB infected young citrus trees in Guangdong 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. Unfortunately, some farmers do not understand……

2 years

3 years 1 year

Picture from Xiaoling Deng Possibility of the root transmission of HLB

HLB was not transmitted by the 36.67% healthy plants became infected trees to healthy citrus when infected 1 year after root grafting they were planted directly together with the infected plants. even after 3 years.

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 1 Treated 2 method of the infected stumps

3 4

5 Picture from Xianjin Bai 3.5 Management of the vector- Asian citrus psyllids 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.  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 Aerosol sprayer Spray result • Aerosol spray is recommended in Guangxi. • Cost: 225 ($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”

Future solution aims at the pathogen: GMO?

Murraya exotica: immune to HLB

Murraya exotica

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 [email protected] [email protected]