Advances in citrus propagation in Brazil

Citriculture is an important agricultural activity worldwide, occupying a relevant position in Brazil among fruit tree production for both the fresh fruit market and the processing industry for concentrated orange juice export. Recent advances in the country’s citrus nursery tree production system have been essential to guarantee the efficiency and competitiveness of Brazilian citriculture. The implementation of strict laws and regulations to produce trees in protected environments and improvements in production techniques for basic citrus propagation materials and nursery trees in São Paulo state has excluded the insect vectors of destructive diseases such as citrus variegated chlorosis and huanglongbing, making this an innovative reference system for citrus propagation around the globe. The main aspects of these advances are presented and discussed in this review, including advances in propagation techniques, scion and rootstock selection, genetic characterization and certification, tree size standards, cultural practices such as irrigation and fertilization for the production of citrus propagation materials and nursery trees, and nursery management tools.

Index terms
Citrus spp.; basic material; nursery tree production; budwood increase blocks

Authorship

Sérgio Alves de Carvalho

Dr., Pesquisador Centro de Citricultura “Sylvio Moreira”, IAC. Rodovia Anhanguera, Km 158, Caixa Postal 04, CEP: 13490-970 –Cordeirópolis-SP. E-mail: sergio.carvalho@ccsm.br Centro APTA Citros Sylvio Moreira, Instituto Agronômico (IAC)BrasilCordeirópolis, SP, Brasil Dr., Pesquisador Centro de Citricultura “Sylvio Moreira”, IAC. Rodovia Anhanguera, Km 158, Caixa Postal 04, CEP: 13490-970 –Cordeirópolis-SP. E-mail: sergio.carvalho@ccsm.br

http://orcid.org/0000-0001-5617-8295

Eduardo Augusto Girardi

Dr., Pesquisador Embrapa Mandioca e Fruticultura, Cruz das Almas-BA, Brasil. E-mail: eduardo.girardi@embrapa.br Embrapa Mandioca e FruticulturaBrasilCruz das Almas, BA, Brasil Dr., Pesquisador Embrapa Mandioca e Fruticultura, Cruz das Almas-BA, Brasil. E-mail: eduardo.girardi@embrapa.br

http://orcid.org/0000-0003-4839-5227

Francisco de Assis Alves Mourão Filho

Dr., Professor Universidade de São Paulo (Esalq). Piracicaba-SP, Brasil. E-mail: francisco.mourao@usp.br Universidade de São PauloBrasilPiracicaba, SP, Brasil Dr., Professor Universidade de São Paulo (Esalq). Piracicaba-SP, Brasil. E-mail: francisco.mourao@usp.br

http://orcid.org/0000-0001-8950-9513

Rhuanito Soranz Ferrarezi

Dr., Professor University of Florida, Indian River Research and Education Center., Fort Pierce, FL, USA. E-mail: rferrarezi@ufl.edu University of FloridaEstados UnidosFort Pierce, Estados Unidos Dr., Professor University of Florida, Indian River Research and Education Center., Fort Pierce, FL, USA. E-mail: rferrarezi@ufl.edu

http://orcid.org/0000-0002-6873-7995

Helvécio Della Coletta Filho

Dr., Pesquisador Centro de Citricultura “Sylvio Moreira”, IAC. Cordeirópolis-SP, Brasil. E-mail: hdcoletta@ccsm.br Centro APTA Citros Sylvio Moreira, Instituto Agronômico (IAC)BrasilCordeirópolis, SP, Brasil Dr., Pesquisador Centro de Citricultura “Sylvio Moreira”, IAC. Cordeirópolis-SP, Brasil. E-mail: hdcoletta@ccsm.br

http://orcid.org/0000-0002-1382-4629

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (4)
Tables (5)

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Figure 1
Differences in seed and leaf morphology, as well as electrophoretic profile for rootstocks with trifoliate leaves: citrange (CT), Poncirus trifoliata (TR), ‘Swingle’ citrumelo (WS) and Citrandarin (CI). A) Similarity in leaf morphology and variation in seed morphology of different materials. B) Electrophoretic profile of the PCR using random primers - RAPD. Different selections of citrandarins. Photos: Helvécio Della Coletta Filho.

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Figure 2
Morphological and molecular comparisons of the main varieties of mandarins used as rootstocks. A) Leaves of the mandarins Cleopatra (CL), ‘Sunki Maravilha’ (SM), ‘Sunki Tropical’ (STr), ‘Sunki Tietê’ (ST), and commom ‘Sunki’ (SK). B) Electrophoretic profile of PCR obtained with microsatellite primers - SSR. Photos: Helvécio Della Coletta Filho.

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Figure 3
Production of citrus buds and nursery trees under screenhouses: A and B) basic plants in pots; C) mother trees in soil; D) budwood increase blocks in soil; E and F) budwood increase blocks in pots; G) seedbed; H and I) rootstock in cone-shaped containers at transplanting; J) rootstock in bags at the grafting point; K and L) grafting; M and N) Grafted trees; O and P) single-stem nursery trees ready for planting (Photos: Sérgio Alves de Carvalho).

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Figure 4
Irrigation systems used in commercial citrus nurseries for the production of rootstock seedlings, nursery trees and budstick in budwood increase blocks: A) shower head, hose nozzle or rain wand (Photo: Rhuanito Soranz Ferrarezi); B) perforated PVC pipes (Photo: Conan Ayade Salvador); C) micro sprinklers; D) spray bars; E) drip system; F) ebb-and-flow subirrigation (Photos: Rhuanito Soranz Ferrarezi) and G) Mobile bar in budwood block (Photo: Sérgio Alves de Carvalho).

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Table 1
Maturation time of sweet oranges, mandarins, acid and sweet limes, lemon and grapefruit cultivars cultivated in Brazil.

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Table 2
Rootstock cultivars used in the production of citrus trees in nurseries of the State of São Paulo, from1970 to 2000 (POMPEU JR. (2005), 2009 to 2015 (POMPEU JR. e BLUMER, 2016) and in 2016 (SETIN, 2017).

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Table 3
Primers selected in research studies (COLETTA-FILHO et al., 1998; CRISTOFANI-YALY et al., 2003; 2011) and currently used in the genetic certification processes at the Campinas Agronomic Institute’s Sylvio Moreira Citrus Research Center.

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Table 4
Major citrus diseases caused by grafting-transmissible pathogens and available diagnostic tests.

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Table 5
Foliar nutritional guidelines for rootstock liners of ‘Rangpur’ lime, ‘Swingle’ citrumelo, ‘Cleopatra’ and ‘Sunki’ mandarins, and grafted trees of ‘Pera’ sweet orange on ‘Sunki’ mandarin and ‘Valencia’ sweet orange on ‘Swingle’ citrumelo at the end of the first growth flush and before the final pruning. Adapted from Bataglia et al. (2008).

Figure 1 Differences in seed and leaf morphology, as well as electrophoretic profile for rootstocks with trifoliate leaves: citrange (CT), Poncirus trifoliata (TR), ‘Swingle’ citrumelo (WS) and Citrandarin (CI). A) Similarity in leaf morphology and variation in seed morphology of different materials. B) Electrophoretic profile of the PCR using random primers - RAPD. Different selections of citrandarins. Photos: Helvécio Della Coletta Filho.

Figure 2 Morphological and molecular comparisons of the main varieties of mandarins used as rootstocks. A) Leaves of the mandarins Cleopatra (CL), ‘Sunki Maravilha’ (SM), ‘Sunki Tropical’ (STr), ‘Sunki Tietê’ (ST), and commom ‘Sunki’ (SK). B) Electrophoretic profile of PCR obtained with microsatellite primers - SSR. Photos: Helvécio Della Coletta Filho.

Figure 3 Production of citrus buds and nursery trees under screenhouses: A and B) basic plants in pots; C) mother trees in soil; D) budwood increase blocks in soil; E and F) budwood increase blocks in pots; G) seedbed; H and I) rootstock in cone-shaped containers at transplanting; J) rootstock in bags at the grafting point; K and L) grafting; M and N) Grafted trees; O and P) single-stem nursery trees ready for planting (Photos: Sérgio Alves de Carvalho).

Figure 4 Irrigation systems used in commercial citrus nurseries for the production of rootstock seedlings, nursery trees and budstick in budwood increase blocks: A) shower head, hose nozzle or rain wand (Photo: Rhuanito Soranz Ferrarezi); B) perforated PVC pipes (Photo: Conan Ayade Salvador); C) micro sprinklers; D) spray bars; E) drip system; F) ebb-and-flow subirrigation (Photos: Rhuanito Soranz Ferrarezi) and G) Mobile bar in budwood block (Photo: Sérgio Alves de Carvalho).

Table 1 Maturation time of sweet oranges, mandarins, acid and sweet limes, lemon and grapefruit cultivars cultivated in Brazil.

Variety

Jan.

Feb.

Mar.

Apr.

May.

Jun.

Jul.

Aug.

Sep.

Oct.

Nov

Dec.

Lima and Piralima

Hamlin

Shamouti

Baia/Baianinha

Westin

Rubi

Valencia Argentina

Valencia Americana

Pineapple

Seleta

João Nunes

Pera

Lima Verde

Lima Sorocaba

Lima Tardia

Valencia

Natal

Charmute de Brotas

Folha Murcha

Variety

Jan.

Feb.

Mar.

Apr.

May.

Jun.

Jul.

Aug.

Sep.

Oct.

Nov

Dec.

Ponkan

Mexerica-do-Rio

Cravo Tangerine

Clementina

W Murcott Tangor

Dekopon Tangor

Montenegrina murcot

Murcott Tangor

Variety

Jan.

Feb.

Mar.

Apr.

May.

Jun.

Jul.

Augo.

Sep.

Oct.

Nov

Dec.

Galego Acid lime

Tahiti Acid lime

Pérsia lime

Sicilian lemon

Marsh Seedless grapefruit

^Source
Adapted from Pio et al. (2005)

Table 2 Rootstock cultivars used in the production of citrus trees in nurseries of the State of São Paulo, from1970 to 2000 (POMPEU JR. (2005), 2009 to 2015 (POMPEU JR. e BLUMER, 2016) and in 2016 (SETIN, 2017).

Rootstock	1970	1988	2000	2009	2014	2015	2016
	(% total plants)
Rangpur lime	99.1	65.0	74.9	48.0	53.0	35.0	33.0
Swingle citrumelo	0.0	0.9	6.0	25.0	32.0	39.0	50.0
Cleopatra mandarin	0.3	27.7	13.7	15.0	1.6	1.2	1.2
Sunki mandarin	-	1.3	1.1	4.9	10.4	3.8	11.9
Volkamer lemon	-	0.7	1.0	2.4	0.7	-	-
Poncirus trifoliata	0.2	0.7	2.3	3.8	1.4	-	3.8

Table 3 Primers selected in research studies (COLETTA-FILHO et al., 1998; CRISTOFANI-YALY et al., 2003; 2011) and currently used in the genetic certification processes at the Campinas Agronomic Institute’s Sylvio Moreira Citrus Research Center.

Primers	Sequence	Category	Group of differentiated rootstocks
OPR04	CCCGTAGCAC	Random	Rangpur limeand Volkamer lemon
AB18	CTGGCGTGTC	Random	P. trifoliataand hybrids
M04	GGCGGTTGTC	Random	P. trifoliataand hybrids
M15	GACCTACCAC	Random	P. trifoliateand hybrids
CCSM 6R CCSM 6F	CCTCTATTAATGTGCCTG ATCTGTGTGAGGACTGAA	Microsatellite	Mandarins

Table 4 Major citrus diseases caused by grafting-transmissible pathogens and available diagnostic tests.

Disease	Pathogen	Acronym	Transmission	Biological indexing*	Other tests most commonly used
Disease	Pathogen	Acronym	Transmission	Biological indexing*	Test**	References
With occurrence in Brazil
Tristeza	Citrus tristeza virus	CTV	Aphids	Galego acid lime	ELISA; RT-PCR; RT-qPCR; Western Blot	BULLETIN OEPP/EPPO (2004)
Psorosis	Citrus psorosis virus	CPsV	Grafting, vectors ?	Laranja do Céu sweet orange	ELISA;RT-PCR;RT-qPCR	EIRAS ET al., 2009; LOCONSOLE et al.(2010); ROY et al. (2005)
Exocortis	Citrus exocortis viroid	CEVd	Grafting, mechanics	Etrog Cidra	imprint hybridization,RT-PCR	EIRAS et al.(2009); LIN et al.(2015)
Xyloporosis	Citrus cachexia vírus Hop stunt viroid	CCaVd HSVd	Grafting, mechanics	Clemelin 1120 Tangor	RT-PCR;RT-qPCR	EIRAS et al. (2009); LIN et al.(2015)
Decline	Not determined		Roots’Grafting		Water injection, Zn trunk content, microscopy, ELISA and PCR	PAIVA et al. (1997); CARVALHO et al (2005)
‘Vein enation’/ ‘Wood gall’	‘Wood gall Vírus’(?)	CVEV	Grafting, Aphids	Volkamer lemon Palermo, Galego Acid lime, and Sour orange	ROISTACHER (1991) EUROPEAN (2017)
Cristacortis	Likely viral origin	____	Grafting	Orlando tangelo	ROISTACHER (1991)
Citrus Sudden death - CSD	Likely viral origin	____	Grafting, vectors ?	Rangpur lime as rootstock	CARVALHO et al. (2005)
Citrus variegated chlorosis - CVC	Xylella fastidiosa	XF	Grafting, Little grig		ELISA, DIBA, PCR, qPCR	BULLETIN OEPP/EPPO (2016)
Huanglongbing (ex greening) - HLB	Candidatus Liberibacter sp.	CLas	Grafting, Vector	Galego, Mandarins	PCR, qPCR	BULLETIN OEPP/EPPO(2014)
Not yet described in Brazil
	Citrus bark cracking viroid	CBCVd	Grafting	No information	SDS-PAGE; Northen	MURCIA et al., 2009
	Citrus bent leaf viroid	CBLVd	Grafting	No information	RT-qPCR	WANG et al.(2009)
	Citrus dwarfing viroid	CDVd	Grafting	No information	SDS-PAGE; Northen	MURCIA et al.(2009)
	Citrus leaf blotch virus	CLBV	Grafting	No information	RT-PCR; RT-qPCR	VIVES et al.(2002); RUIZ-RUIZ et al.(2009)
	Citrus variegation virus	CVV	Grafting	No information	RT-PCR; RT-qPCR	ROY et al. (2005); LOCONSOLE et al.(2010)
	Citrus leaf rugose virus	CLBV	Grafting	No information	RT-PCR	ROY et al. (2005)
	Citrus tatter leaf virus	CTLV	unknown	Rusk Citrange	RT-PCR	ROY et al. (2005)
	Citrus yellow mosaic virus	CYMV	Grafting, mechanics	No information	ELISA; RT-PCR	ROY et al. (2005)
	Indian citrus ringspot virus	ICRSV	Grafting	No information	RT-PCR	ROY et al. (2005)
Stubborn	Spiroplasma citri	____	Grafting, Vector	___	ELISA; PCR; qPCR	NEJAT et al., 2011; WANG et al. (2015)

^*
Indicator plant most used for the biological test, according to MACCHERONI et al. (2005) for MSC, CARVALHO et al. (2001b) for CVMV (Volkameriano Palermo), and ROISTACHER (1991) for the other CVEV indicators and other viruses.
^**
Acronym Meaning: RT - PCR: reserve transcriptase followed by PCR; RT-qPCR: reserve transcriptase followed by quantitative real-time PCR; ELISA: Enzyme Linked ImmunonoSorbent Assay; DIBA: Dot Immunoblot Assay; SDS-PAGE: Sodium dodecyl sulfate polyacrylamide gel electrophoresis'.

Table 5 Foliar nutritional guidelines for rootstock liners of ‘Rangpur’ lime, ‘Swingle’ citrumelo, ‘Cleopatra’ and ‘Sunki’ mandarins, and grafted trees of ‘Pera’ sweet orange on ‘Sunki’ mandarin and ‘Valencia’ sweet orange on ‘Swingle’ citrumelo at the end of the first growth flush and before the final pruning. Adapted from Bataglia et al. (2008).

Nutrient	Rootstock liners		Grafted trees ‘Pera’ on ‘Sunki’ and ‘Valencia’ on ‘Swingle’
	‘Rangpur’ ‘Cleopatra’ and ‘Sunki’	‘Swingle’	End of the first growth flush	Before the final pruning
	-------------------------- g/kg --------------------------
N	25 – 35	30 –40	35 – 40	30 – 40
P	2.0 – 2.5	2.2 – 2.8	2.2 – 2.8	2.0 – 2.4
K	15 – 20	16 – 22	22 – 26	21 – 28
Ca	20 – 30	25 – 35	16 – 23	20 – 27
Mg	2.7 – 3.8	3.5 – 4.5	2.8 – 4.1	2.3 – 3.5
S	2.5 – 3.5	3.0 – 4.5	2.5 – 3.5	2.9 – 3.7
	--------------------------mg/kg--------------------------
B	50 – 120	90 – 150	55 – 110	90 – 170
Cu	5 – 30	5 – 30	5 – 30	10 – 30
Fe	100 – 200	100 – 200	100 – 200	120 – 250
Mn	50 – 200	100 – 250	40 – 200	70 – 180
Zn	20 – 70	25 – 70	25 – 55	40 – 90

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Sociedade Brasileira de Fruticultura Via de acesso Prof. Paulo Donato Castellane, s/n , 14884-900 Jaboticabal SP Brazil, Tel.: +55 16 3209-7188/3209-7609 - Jaboticabal - SP - Brazil
E-mail: rbf@fcav.unesp.br

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Advances in citrus propagation in Brazil

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[TFN0101] ^Source
Adapted from Pio et al. (2005)