South African Journal o f Agricultural Science

Volume 1, N um ber 4, D ecem ber , 1958

T he G overnm ent P rinter, Pretoria.

XYLOPOROSIS, CACHEXIA AND ABNORMAL BUD-UNIONS

IN SOUTH AFRICAN CITRUS TREES
(M e t opsomming in Afrikaans)
(A vec resum e en Frangais)

------ ♦------

A. P. D. M cC L E A N and A. H . P. E N G E L B R E C H T , Division of P lan t Pathology,

Pretoria

A bstra ct
Tn rootstock experim ents in South A frica the trees form ed from scion varieties on sweet lime
stocks have usually perform ed badly. T he extrem e stunting o f som e o f the scions and the type oi
pitting in the sweet lim e stocks un d er them is strong evidence for the occurrence o f xyloporosis
virus in such scions. T he presence o f the virus in tw o scions—a L isbon lem on and a E ureka lem on—
was confirm ed by a n inoculation test to seedlings o f the O rlan d o tangelo.
Exam ples o f ab n o rm al unions in citrus trees o f various scion/stock com binations are described
from S outh A frica. T hey are sim ilar to those reported from other countries.

I n t r o d u c t io n
X yloporosis, a bud-transm issible virus infection o f citrus trees has now been
reported from m ost countries growing citrus. The evidence indicates th at this virus
is carried in m any commercial varieties. A disease o f the O rlando tangelo called
cachexia is probably caused by the same virus.
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A num ber o f abnorm al bud-unions have been described in trees form ed from
com binations o f some scions and some rootstocks. O f these the best known is the
one occurring in trees o f sweet orange on rough lemon roots. The exact causes of
the abnorm al unions are not know n though there is evidence th a t some o f them are
due to virus infection.
The object o f this article is to place on record the occurrence o f these infections
and disorders in South Africa. The evidence to be presented is from observations
on the behaviour o f trees in ro otstock experim ents and in commercial orchards,
and on the results o f one transm ission experim ent. The rootstock experim ents,
which are under the direction o f D r. R. H . M arloth, are projects o f the C itrus and
Sub-Tropical H orticultural Research Station, N elspruit. The scion m aterial used
in the ro otstock experim ents came from parent trees in the variety collection o f
the Station.
X y l o p o r o s is (C a c h e x ia )

X yloporosis was described from Israel (R eichert & Perleberger, 1934) as a disease
o f citrus trees on sweet lime stocks. C achexia was described later from F lorida as a
disease o f the O rlando tangelo (Childs, 1950). The two are thought to be caused by
the same virus, because o f a sim ilarity in sym ptom s and because in reciprocal
transm issions the one disease has been reproduced from the other (Childs, 1956).
Cachexia is also thought to be the cause in F lorida of an abnorm al bud-union found
in association w ith m any sweet oranges on rough lem on stocks (G rim m , G ran t &
Childs, 1955). Recently in Brazil a clonal line of Pera orange, said to be free of
xyloporosis, was reported to produce bud-union sym ptom s on rough lem on similar to
R eceived fo r p u b lic a tio n on 18 June, 1958

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL B U D -U N IO N S IN SOUTH AFRICAN CITRUS TREES

the one in F lo rid a (G rant, M oreira & C osta, 1957). The opinion was given from this
evidence that either xyloporosis and cachexia are different viruses or that xyloporosis
(cachexia) virus is not the cause o f the abnorm al bud-union in trees o f sweet oranges
on rough lem on. M ore transm ission experim ents seem necessary to clarify the
position.
X yloporosis causes abnorm al changes in the wood and bark. Peg-like o u t­
grow ths, consisting o f phloem -like elements in place o f xylem develop from the inner
face o f the b ark and ju t into the w ood (W inocour, 1956). W hen rem oved the pegs
leave in the w ood pit-like depressions. In sweet lime stocks o f affected trees the
vascular pits and pegs are described as conoid and are said to be m ost num erous
just below the bud-union. In later stages the w ood may assume a perforated or
sieve-like appearance (D u C harm e, 1951). Sim ilar sym ptom s are produced in
O rlando tangelo by cachexia but the pits and corresponding projections are irregular
and n o t always conoid. In b o th diseases gum pockets develop in the bark o f sensitive
species and the phloem m ay show a brow n discoloration.
F ro m the inform ation available the trees m ost sensitive to xyloporosis are those
on the stocks of sweet lime. The genera) effect o f the disease on the trees is a m arked
stunting o f the scion and prem ature decline. O bservations in F lorida and Texas
show th a t the varieties m ost sensitive to cachexia are to be found am ongst the
m andarins, m an d arin hybrids (tangelos), kum quats and k u m quat hybrids (Childs,
1951, 1956; Olson, 1954; Olson & Shull, 1956).
The severity o f the diseases caused by xyloporosis and cachexia depends on the
com position o f the tree. In general when one com ponent o f the tree is a sensitive
variety, w hether it be rootstock or scion, then the tree becomes stunted and declines
at an early age. M any citrus species and varieties, including m ost sweet oranges,
grapefruits and sour orange seem to possess good tolerance and a p a rt from mild
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pitting th a t develops in some o f them , are apparently unharm ed by the virus. They
grow well either as seedling trees or when budded on the roots o f a tolerant stock.
B oth xyloporosis and cachexia are bud-transm issible. N o insect vector is know n
but there is evidence from F lo rid a th at cachexia may be transm itted through the
seed (Childs, 1956).
The m ain difficulty in studying these viruses is the absence o f a quick reacting
indicator. The best available indicator at present for cachexia is the O rlando tangelo,
but sym ptom s in inoculated seedlings take as long as tw o to three years to develop.
W hen scions affected with xyloporosis are budded on sweet-lime stocks they m ay
grow well at first, but the sym ptom s o f disease in the scion and stock do not become
evident for a few years.

E v id e n c e f o r o c c u r r e n c e o f x y l o p o r o s is a n d c a c h e x ia in South A f r ic a n c it r u s

Behaviour o f scion varieties on sw eet-lim e stock

The sweet lime has never been used com m ercially as a rootstock in South A frica
but has been tried in rootstock experim ents w ith unsatisfactory results. M cClean
(19506) drew atten tio n to this and thought the failure was due to virus infection.
He noted the extrem e dwarfing o f some scions and the presence o f pits in the w ood
o f the sweet lime stocks sim ilar to th a t reported from Israel in trees affected with
xyloporosis. On this evidence and the fact th a t trees were found to contain tristeza
(stem -pitting) he (1950a) suggested that xyloporosis and tristeza (stem -pitting) m ight be
caused by the same virus. This proved incorrect and m ore recent evidence has
shown that the two are caused by different viruses (Childs, 1952). The two viruses,
however, often exist together in the same tree. M arlo th (1957) reporting on the

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 A. P . D. MCCLEAN AND A. I-L P . ENGELBRECH T

behaviour o f Sham outi and T om ango oranges, noted the failure and prem ature
decline o f these scions on sweet lime, Poncirus trifoliata and other stocks. H e
attrib u ted the failures to xyloporosis. As further evidence for the occurrence of
this virus he n o ted the developm ent o f various types o f pitting in b o th scions and
rootstocks. In his report on rootstocks for grapefruit, M arloth (1958) writes th at
a num ber of stocks proved unsuitable at an early age, either failing within a few years
or resulting in only dw arfed trees. H e also noted th at even on other stocks (including
sweet orange and rough lemon), all trees declined at from 15 to 18 years from planting.
H e considered the early decline to be associated w ith the presence o f bud-transm issible
exocortis and xyloporosis, apart from the insect-transm itted stem -pitting virus in
the scion m aterial. H e offered no evidence to support this statem ent.

T a b l e 1.—Behaviour of some scion varieties on sweet lime stocks

T a b e l 1. — Gedrag van som m ige bostam varieteite op soetlem m etjie-onderstam m e

Age
N o. of in Height
Scion varieties trees years in feet C ondition
Bostani varieteite Aantal Ouder- Hoogte Toestand
borne domme in voet
in jare

(1) V alencia..................... 24 12-18 4 -6 '

W ashington N avel
Washington-Nawel. . 12 12 5-7 i* Severely stunted a n d decline
Erg verdwerg en verswak
T om ango orange
Tomangolemoen........ 4 16 4 -6 „
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P reto ria N avel I Stunted a n d declining b u t less severe

Pretoria-N awel . . . . 16 18-21 5-9 Verdwerg en verswak, maar minder ernstig
M arsh grapefruit Severely stu n ted a n d decline
M arsh-pom elo........... 6 12 5-6 Erg verdwerg en verswak
Lisbon lemon Sem i-dw arfed— fa ir condition
Lissabonlemoen........ 9 15 7-8 / Halfverdwerg— redelike toestand

(2) W est Indian lime ] Well grown, now in state o f decline

Wes-Indiese lemme- 3 17 13-14 f- Goed uitgegroei maar nou in toestand van
tjie agteruitgang
im p re s s m andarin 1 Severely declined
Empress-nartjie......... 1 17 9 Erg verswak
K um quat 1 T hree with severe decline; 1 fair
K um kwat.................... 4 17 5-10 r Drie erg verswak; 1 redelik
1 One fairly good— other declining
M inneola ta n g e lo ... 2 12 10-12 ► Een redelik goed, die ander besig om agteruit
te gaan
O w ari satsum a . . . 3 12 5-9 '
H am lin orange
Hamlinlemoen........... 4 12 6-7
V alencia..................... 8 12 5-9
M arsh grapefruit Stunted and severe decline
M arsh-pom elo........... 3 16 4-5 r Verdwerg en erg verswak
T riu m p h grapefruit
Triumph-pomelo.. . 3 16 4-5
Ellen grapefruit
Ellen-pomelo............. 3 16 4-5 j

(1) T rees in rootstock experim ents—planned for quantitative inform ation

(2) Trees in sm all scale plantings— for observation only
(1) Borne in omlerstamproewe—beplan vir kwantitatiewe gegewens
(2) Bomc in klein aanplantings— vir waarneming alleen

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BU D -U N IO N S IN SOUTH AFRICAN CITRUS TRE ES

Some observations on the behaviour of different scion varieties on sweet lime

stocks in the rootstock experim ents o f the N elspruit Station are given in Table 1.
The group o f trees o f each scion variety is the progeny o f a single paren t tree growing
in the variety collection o f the N elspruit Station, These parents in turn originated
from others selected some years previously from com m ercial orchards, with the
exception o f H am lin orange, M inneola tangelo and Owari satsum a, which were
im ported directly from overseas. The results show a consistent failure o f trees
on this stock. One tree o f M inneola tangelo is still in fairly good condition after
12 years but is an exception. The rem ainder are for the m ost p a rt stunted, with
short twigs, and show deficiency sym ptom s and die-back.

A variety o f abnorm alities o f the vascular tissues were observed in the trunks
o f the trees by rem oving a strip o f b ark across the union. The abnorm alities were of
two types: projections from the cambial face o f the bark th a t fitted into corresponding
depressions (pits) in the underlying wood, and hair-like projections (extensions o f
the m edullary rays) ju ttin g from the surface o f the wood into the bark. In the latter
case when the b ark is rem oved from the wood its inner face shows a num ber o f small
holes and hence the expressions o f pin-holing and honey-com bing, coined by some
authors to describe this sym ptom . M edullary ray projections are n o t specific for
xyloporosis and have been reported in association w ith w ood-pocket disease o f
lem ons and seedless lime (Calavan, 1957), and with tristeza disease in trees on sour
orange stocks (D u C harm e & K n o rr, 1954). Their developm ent seems to be a
secondary effect associated with trees that are p o o r and in a state o f decline.

The sweet lime stocks o f m ost trees exam ined showed m edullary ray projections.
They were n o t particularly plentiful, b u t were com paratively large and tended to
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

break off and rem ain in the cavities when the b ark was peeled from the wood. In
addition the stocks showed projections from the bark with depressions or pits in
the wood (Plate I, Fig. 2). The projections were either narrow and ridge-like or
short and m ore conoid in shape. U nder tops like M inneola, Owari satsum a, Empress
m andarin, k u m q u at and the P retoria Navel orange the projections seemed to be
m ostly in the form o f ridges (Plate I, Fig. 5). U nder others like Valencia, Hamlin
orange, Lisbon lemon and grapefruit both types o f projections were observed.

M ost o f the scions also showed m edullary ray projections. They were plentiful
in the trunks o f Owari satsum a, Em press m andarin and k u m quat (Plate I, Fig. 4).
In one tree o f O w ari satsum a the projections from the wood continued up the trunk
into the branches. M edullary projections were also observed in the scion p a rt of
the trunks o f the Valencias and other sweet oranges. The W est Indian limes and
grapefruits showed the m ost prom inent projections from the b ark with corresponding
deep channels in the wood. In other trees there was evidence o f only slight bulges
from the surface o f the bark. The H am lin orange showed a few small conoid (or
deltoid) projections.

The stocks of m any of the stunted sweet oranges and especially of the older
Valencias showed an orange-brow n discoloration o f the wood and inner face o f the
bark. The discoloration seemed to sta rt from the union and to spread dow n the
trunk with the deterioration o f the tree. The stocks often show longitudinal cracks
in the bark, and the cracks m ay extend through into the w ood (Plate 1, Fig. 2 & 3).
In advanced stages a large area o f the bark m ay dry out and shell off, accom panied
by decay o f the underlying wood. The same sym ptom s are noted by Reichert and
Perleberger (1934) and D u C harm e (1951).

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 A. P . D. MCCLEAN AND A. H. P . ENGELBRECHT

The p oor perform ance of citrus trees on sweet lime stocks in South A frica
could be due to two viruses: xyloporosis and tristeza. F rom their observations in
Brazil, G ran t, C osta & M oreira (1951), state th at sweet oranges on sweet lime infected
with tristeza decline slowly and eventually show typical sym ptom s of tristeza, although
this m ight take several years. In South A frica tristeza in one or other o f its forms
occurs in all orchard trees and has been isolated from all trees on sweet limes th at
have been tested. There seems little d o u b t th at this virus has been a contributing
cause o f the p o o r perform ance an d ultim ate decline o f scions on this stock and in
some cases m ay have been entirely responsible. To w hat extent xyloporosis has
contributed to the failure will not be know n with certainty until inoculation tests
to a suitable indicator have shown which scions carry xyloporosis, and until a
com parison has been m ade o f the grow th on sweet lime stocks o f scions free of
xyloporosis and those infected w ith it.
X yloporosis is thought to be present in some o f the scions used in the rootstock
experim ents, such as the V alencia, W ashington Navel, the three varieties o f grape­
fruit, and the Lisbon Lem on. Evidence for this is the unhealthy condition and
severe stunting of m ost of the trees on sweet lime stocks (Plate I, Fig. 1), and the type
o f pitting in the stock p art o f the trunks (Plate I, Fig. 2). But we are not on sure
ground in using types of vascular pits and projections, except possibly those associated
w ith the sweet lime itself, as an aid in diagnosis.

Transmission test to seedlings o f Orlando and M inneola tangelos

Evidence for the occurrence o f cachexia virus in South A frica comes from the
following experim ent, designed originally to test the behaviour o f O rlando and
M inneola tangelos to tristeza virus. Seedlings o f the two varieties were inoculated
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

by grafting from six sources of the virus, differing from one another in the reaction
induced in indicator seedlings (sour lime, sour orange, grapefruit, and com posite
trees of sweet orange on sour roots). F o u r of the sources were orchard trees. The
other two were seedlings in which virus had been recovered from orchard trees by
means o f aphids ( T oxoptera citricidus). The test trees were seedlings plus a daughter
tree o f each one prepared by grafting a piece o f the seedling into the stum p o f a
decapitated seedling of rough lem on. Three seedlings o f each variety together w ith
their respective daughter trees on rough lem on stocks, am ounting to a total o f 12,
were inoculated from each source of infection.
A t the start the test trees were in pots w ithin a glasshouse, where they were
under observation for 20 m onths. In this period w ith the exception o f a few suffering
from ro o t decay they rem ained in good condition, and the inoculated ones grew
as well as the untreated controls. A third o f the seedlings inoculated from the navel
orange and the two lem ons developed a few vein swellings on their leaves, a reaction
to vein enation virus know n to be present in these three trees. Some of the orlandos
inoculated from the navel orange showed an occasional cleared zone in the veins
o f new leaves, otherwise the only visible reaction to tristeza virus was shown by the
series inoculated from the M arsh 706 isolate. All the orlandos in this series developed
well defined fleckings (cleared zones) in the veins of their new leaves, together with
fairly extensive pitting in the w ood (the type o f pitting resembled th at induced in
grapefruit and sour lime by tristeza virus). O f the m inneolas only one of the seedlings
together with its daughter tree on rough lem on stock developed leaf fleckings and
w ood-pitting. Sub-inoculations from all the test trees to indicator seedlings confirm ed
th at they had been successfully infected, irrespective o f w hether they had sym ptom s
or not, and that in each case the type o f infection was the same as that introduced
from the source tree.

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BUD -UNIONS IN SOUTH AFRICAN CITRUS TREES

A fter 20 m onths the test trees, except a few p o o r ones, were transplanted into
the open. Eighteen m onths later sym ptom s sim ilar to those described for cachexia
by Childs were showing in the trees o f the two series inoculated from the lemon
sources. The other trees were norm al. This position has rem ained unchanged
through another growing season (Table 2). It is interesting to record th a t the
sym ptom s o f w ood-pitting in the seedlings o f O rlando and two o f the m inneolas
infected from the M arsh 706 isolate have disappeared with the subsequent grow th
since the trees were transplanted in the field.

T a b le 2.—R eaction of seedlings of O rlando and M inneola tangelos to virus in

different orchard trees, introduced by grafting
T a b e l 2.— R eaksie van Orlando- en M inneola-tangelo's teenoor virusse w at deur
enting uit verskillende borne verkry is

Test N o. o f N o. with
Sources o f infection * seedlings trees cachexia
Bron van besmelting * Proef- Aantal A antal met
saailinge bome kacheksie

P ickstone N avel— Tree in variety collection : N e lsp ru it.........") O rlando 6 0

Pickstone-Nawel—Boom in die varieteitsversameling: Nelspruit f M inneola 6 0
L isbon lem on—T ree in variety collection: N e lsp ru it............. ]
Lissabonsuurlemoen— Boom in die varieteitsversameling: Nel- }► O rlando 5 5
M inneola 6 6
spruit J
Cecily grapefruit t — Tree in private orchard ................................\ O rlando 5 0
Cecily-pomelo t — Boom in private boord
E ureka lem on— T ree in private o rc h a rd ........ ................................ \
> M inneola
O rlando
4
6
0
6
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Eureka-suurlemoen— Boom in private boord M inneola 6 6

M arsh grapefruit (706) i — Isolate recovered in an orange seed-S
ling by aphides O rlando 4 0
Marsh-pomelo (706) +— Isolasie verkry uit ’n lemoensaailing [" M inneola 5 0
deur piantluise J
W est Indian lime— Isolate recovered in a lime seedling b y l
aphides 1 O rlando 5 0
Wes-Indiese lemmetjie— Isolasie verkry uit ’n leinmetjiesaailing r M inneola 6 0
deur piantluise J
U n treated c o n tro ls................................................ ............................... 1 O rlando 11 0
Onbehandelde kontroles M inneola 10 0

* A ll know n to be sources o f tristeza virus, but sources differing in their reaction to indicator
plan ts
t C ontains a very m ild strain o f stem -pitting (tristeza) virus
t C ontains a very virulent strain o f stem -pitting (tristeza) virus
* Alm al bekencl as bronne van tristeza virus, maar verskil in hid reaksies met indikatorplante
t Bevat ’n swak ras van tristezavirus
t. Bevat ’n baie virulente ras van tristezavirus

The sym ptom s in the trunks of the O rlando tangelos on w hich we base our
diagnosis o f cachexia are as follow s:—
(1) Stunting o f the trees and a general or partial chlorosis o f m any leaves.
The chlorotic p attern on the leaves resembles a deficiency sym ptom and
w as m ore noticeable in the latter p a rt o f the season.
(2) Brow n staining w ithin the b ark tissues, seen by paring off the outer layers.
In some places the brow n stain came through to the inner face o f the
b a rk (Plate II, Fig. 1).

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 A. P. D . MCCLEAN AND A. H. P . ENGELBRECHT

(3) A variety o f small projections from the inner face of the bark— small pegs,
short ridges, and small swellings—with corresponding cavities in the
w ood into which the projections fitted (Plate IT, Fig. 2 & 4).
(4) Peg-like projections from the surface o f the w ood that ju t into the bark
and leave small pin-holes when removed. These are m edullary ray
projections (Plate II, Fig. 5).
(5) Brown gum pockets within the wood, in our trees in which sym ptom s
have been evident for two years, the gum pockets were arranged along
the ring m arking the beginning of the previous season’s growth. R adiating
from the gum pockets through the outer layers o f young wood were broad
m edullary rays, appearing to the eye as light bands across the new w ood
(Plate II, Fig. 3, 4 & 5). The gum pockets in the wood seem to have their
origin m ainly at the starting points o f the m edullary rays or vice versa.
In pieces of stem left to dry the cells in the gum pockets collapse and
cavities are form ed.
The reaction o f O rlando seedlings and their daughter trees on rough lemon
stocks was the sam e except th at in the latter the sym ptom s were confined to the scions.
The sym ptom s were considerably m ilder in the m inneolas. So far the affected
trees are growing as well as the others. The only noticeable change in the trees is
the developm ent o f small projections from the inner face o f the bark and
corresponding depressions in the w ood. N o brow n staining in the b ark or gum
pockets in the w ood have so far been observed, but in some places in the trunks the
surface o f the w ood and inner face o f the bark m ay show a slight yellow discoloration.
These positive results in the inoculation o f orlandos and m inneolas provide
the first p ro o f th at xyloporosis (cachexia) occurs in some o f our orchard trees.
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The apparent absence of the virus in the Pickstone Navel is surprising as this
variety o f orange is one th at shows an abnorm al bud-union on rough lemon, a
sym ptom thought by some to be caused by xyloporosis (cachexia).
It may be o f interest to record here the com parative grow ing perform ance of
the tangelo seedlings and their daughter trees on rough lemon stocks in the above
experim ent, in the first tw o-and-a-half years in the orchard the O rlando seedling
trees have grow n m ore vigorously than the daughter trees on rough lemon stocks,
in some cases the difference in size being striking. This applies only to the series
free o f cachexia. W ith the m inneolas, the difference if any, tends to favour m ore the
trees on rough lem on stocks.

A bnorm al b u d -u n io n s in So u th A f r ic a n c it r u s trees

Sw eet oranges on rough lemon stocks

The first record of sweet oranges showing an abnorm al union on rough lemon
stocks comes from Israel. Y edidyah (1937) and later O ppenheim er (1940) report a
corky fissure at the union o f Sham outi orange on rough lemon stock that, shows
prom inently as a collar round the outside o f the trunk. M ore recently in F lorida
(G rim m e t a l , 1955) m any orch ard trees o f sweet orange on rough lem on have been
observed w ith a groove in the wood along the line o f the union and a toothed ridge
projecting and fitting into the groove from the inner face o f the bark. In such trees
the layer o f functional phloem is described as very thin at the union, where most o f
the phloem is discoloured yellow or brow n and is non-functional.

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BUD -UNIONS IN SOUTH AFRICAN CITRUS TREES

The same internal sym ptom s are also associated w ith the bud-union disorder
of Sham outi orange on rough lem on. (These sym ptom s were pointed out to the
senior au th o r during his visit to Israel in 1956.) The two disorders seem related
and apparently the m ain difference is one o f severity. N o stunting or other ill-effect
on the trees as a whole is reported from F lorida. The inform ation from Israel is
conflicting. Reichert, Yoffe & Bental (1953) reporting on the relative merits o f
rootstocks in relation to their susceptibility to xyloporosis say th at the rough lem on
was a com plete failure under Sham outi orange when grown in a loam y soil. In light
soil they note th at the rough lem on is satisfactory but to a less degree th an trees on
sweet lime. M endel ( 1956) on the oth er hand says th a t the rough lemon “ stock seems
to be well adapted to the Sham outi orange. The ‘ ring ’ is no d o u b t an abnorm ality,
but the vigorous developm ent o f the tree, its health and high yields, do n o t indicate
a pronounced stock-scion incom patibility ” . T he trees reported on by M endel were
grow ing in light soil. M endel notes a tendency for young trees to produce num erous
suckers from the rough lem on stock, probably as a result o f a girdling effect o f the
corky fissure at the union. Otherw ise one assum es from M endel’s report th at the
trees are unharm ed.
In a ro otstock planting in Brazil, G ra n t et al. (1957) recently recorded bud-
union sym ptom s (pegs plus orange coloured ring) in trees o f P era orange on F lorida
rough lem on. Sister trees on trifoliate stock in the same planting showed similar
sym ptom s at the union. This line o f Pera orange was judged to be free o f both
exocortis and xyloporosis on the behaviour o f trees on stocks o f trifoliate orange
and sweet lime.
The abnorm al unions in trees o f sweet orange on rough lemon is thought to be
caused by virus infection. In F lorida trees of the same variety in the same orchard
have been observed w ith and w ithout bud-union symptoms. This seems to rule out
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

the possibility th a t the trouble is due to direct incom patibility. Transm ission tests
to seedlings o f O rlando tangelo in F lorida (Childs, G rim m , G rant, K n o rr & N orm an,
1955) showed th a t a high p ro p o rtio n o f affected trees contain xyloporosis (cachexia),
and this has led to the belief there th a t xyloporosis (cachexia) may be the causal virus.
Reference was m ade earlier to some evidence from Brazil th at throw s possible d o u b t
on this conclusion, if indeed xyloporosis and cachexia are the same virus. A nd it still
rem ains to be explained why in the presence o f xyloporosis (cachexia) one scion like
the sweet orange develops an abnorm al union w ith rough lemon and an o th er like
grapefruit a norm al union.
Sim ilar bud union disorders occur in South Africa to those described from
Israel and F lo rid a (Plate III, Fig. 1, 2 & 3). M arlo th (1938) reported th a t the
Sham outi and T om ango oranges and other related types behave on rough lem on
stocks in the sam e way in South A frica as in Israel, and develop an abnorm al collar­
like ring o f corky tissue round the tru n k along the line o f the union. H e noted a
dw arfing o f the trees o f these varieties and attrib u ted this to a constricting effect at
the union. In a recent publication M arlo th (1957) lists other varieties in the collection
a t N elspruit w ith the sam e sym ptom b u t varying from severe to slight (A ddorosa,
Cadenera, M altese Blood, N atal, H om osassa, R uby Blood, R uby Early, St. M ichael’s
Blood, and V erna). T o this list can be added Vicideo (ex C alifornia), L etaba and
H all’s m id-season varieties (two varieties o f local origin), and a hybrid o f Sham outi
orange and sour orange (ex California).
M arlo th suggests the abnorm al ring is due to virus infection, probably
xyloporosis, because o f occurrence o f types o f pitting in both stocks and scions th at
he regards as sym ptom atic o f xyloporosis virus.

396
 A. P . D . MCCLEAN AND A. H . P. ENGELBRECHT

The interna] groove in Ihe wood along the line of the union with an irregularly
tooth ed ridge fitting into it from the inner face of the bark (Plate III, Fig. 4), and
gum pockets within the bark tissues (Plate III, Fig. 3) seem to be sym ptom s
associated with the same bud-union abnorm ality. They were observed to occur in
the tru n k s of all trees showing the external ring of corky tissue. But some varieties
showed only internal sym ptom s, their tru n k s appearing norm al on the outside.
O thers were interm ediate and showed slight external sym ptom s, as for example,
splitting and corking o f the b ark tissues for a few inches or m ore along the line of
the union. H ere the age o f the tree seems to be a determ ining factor, the external
effects on the bark becom ing m ore pronounced as the trees get older.
In the collection o f sweet oranges a t N elspruit the trees o f 17 varieties on rough
lem on stocks show b o th external and internal sym ptom s, the trees of 22 other
varieties show internal sym ptom s only, and the trees o f 46 norm al unions. O f the
latter 29 were selections from comm ercial orchards in South A frica and in some
cases were probably from parents o f seedling origin. O n sweet stocks the trees of
all varieties have norm al unions.
The trees in the variety collection were the parents o f trees used in rootstock
experim ents and other orchard trials to com pare yield and perform ance o f orange
varieties. The behaviour o f daughter trees on rough lem on stocks in these
experim ents (sum m arised in Table 3) is the same as th at show n by the parents. The
results are consistent: either all the daughter trees o f the scion variety have an
abnorm al union or all a norm al one.
O bservations were also m ade in the orchards o f two large estates: the C rocodile
Valley C itrus E state in the E astern Transvaal and Zebediela Citrus E state in the
N o rth ern Transvaal. A t b o th places the m ajority o f trees 6 f W ashington Navel
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on rough lemon th a t were exam ined showed abnorm al unions. M ostly the trunks
were norm al on the outside an d the sym ptom s were confined to the inside.
O ccasionally in older trees an external corky scar occurred along the line o f the
union either all the way round or p a rt o f the way only. W ell-defined internal
sym ptom s were seen in trees as young as five to six years old. A t Zebediela a few
trees were found th a t h ad norm al unions. W ith Valencias m ost o f the trees exam ined
had norm al unions (Plate III, Fig. 5), but exceptions to this were found at both
Zebediela and C rocodile Valley. In one orchard on the latter estate some large
trees o f V alencia, ab o u t 30 years of age, showed both internal and external sym ptom s.
The external collar o f corky tissue was as m arked in these trees as in those o f
Sham outi orange and related varieties (Plate III, Fig. 1). The trees were still
productive an d in good condition.
In exam ining trees for bud-union sym ptom s a strip o f bark, a few inches long,
was rem oved from the tru n k s across the unions. The exam inations revealed vascular
pits and projections away from the line o f the union and scattered over the cam bial
faces o f w ood and b ark respectively in m ost trees figuring in these observations.
The arrangem ent in m any cases tended to be longitudinal. They were seen in sweet
orange scions and in b o th sweet orange an d rough lemon stocks. Their size, shape,
and frequency varied a lot, even in sister trees. They occurred as frequently in
trees w ith abnorm al bud-unions as in trees w ith norm a] ones. In m ost trees the bark
projections (or corresponding pits in the wood) were small, few in num ber, and either
in the form o f shallow ridges or they were pointed and deltoid in shape. Some trees
o f M editerranean sweet orange showed large projections, either rectangular or
deltoid in shape, from the b ark o f the scion, arranged longitudinally and ending
abruptly a t the union; but other sister trees showed only small ridge-like projections.

397
 XYLOPOROSIS, CACHEXIA AND ABNORMAL BU D -U N IO N S IN SOUTH AFRICAN CITRUS TREES

In the trunks of m ost orange scions pitting was slight b u t in four varieties (M alta
Egg, Pera, Pine and Verna) pitting was extensive and severe th roughout the trunks
and branches and seemed to be m ore of the type associated w ith grapefruit and the
W est Indian lime when infected w ith tristeza [described as channelling by D u C harm e
& K n o rr (1954)].
T a b l e 3 . — O ccurrence o f bud-union abnorm alities in trees on rough lemon stocks
T a b e l 3 . — Voorkoms van entverbindingabnorm aliteite b y borne op growweskilsuur-
lemoen onclerstamme

N o. o f Age
Scion variety trees in years C ondition o f bud-union
Bostamvarieteit Aantal Ouderdom Toestand van die entverbinding
bome in jare

(o) In rootstock experim ents—

In onclerstamproewe—
V alencia................................. 52 16-21 \
H a m lin ................................... Normal/TVormao/
3 12 J
A bnorm al—external and internal sym-
T o m a n g o ............................... 8
17 tom s/ Abnormaal— inwendige en uit-
S h a m o u ti............................... 3 22 J!•
wendige simptome aanwesig
A bnorm al— all w ith internal sym ptom s
1 and som e with external sym ptom s as
W ashtington N a \s\j-n aw el 30 12-18 )■ well j Abnormaal—almal m et inwendige
1 simptome en sommige ook m et uit-
J wendige simptome
Pretoria Navel/-naive/ 16 1 8 -2 H
M editerranean sweet o r­ 6 22 A b n o rm al— internal sym ptom s only/
ange / Mediterreense Abnormaal—slegs inwendige simp­
soellemoen tome
j
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

(b) In an experim ent to com pare

strains o f navel oranges/
In ’n p ro e f waarin die nawel-
seteksies vergelyk word—
W ashington Navel/-«<7ire/. 8 16 1
F ranzina R ust N av el/ 4 16 1 A b n o rm al— Internal sym ptom s o n ly /
-nawel Abnormaal—slegs inwendige simptome
Pretoria Navel/-/;oitW ....... 8 .« r
A b n o rm al— all internal sym ptom s and
Pickstone N avel/-«oive/.. . 4 . « i som e external as well/ Abnormaal—al­
B addaford N aveI/-«oire/. . 8 16 f- m al m et inwendige simptome en som ­
mige ook met nitwendige simptome
C om pany N avel /-navel.. . 8 .6 J N o rm al/N orm aal

(c) In an experim ent to com pare

m id-season varieties///; ’n
p ro e f waarin die midseisoen-
varieteite vergelyk word—
Sham outi, R uby Early, 6 o f each/ 9 A bnorm al— internal and external sym p­
A ddorosa, H all’s, T o­ van elk tom s//! bnormaal— inwendige en uit-
m ango & L etaba wendige simptome
N orris, H am lin, Bailedge 6 o f each/ 9 N o rm a l/Normaal
Early, C lanor, Rico van elk
& M oss
Severe vascular pitting has not been observed in rough lemon stocks in South
A frica, b u t small ridge-like and deltoid projections from the bark and pits in the
w ood to m atch are com m on in rough lem on stocks under a variety o f scions (Plate III,
Fig. 5). They have also been observed in the trunks o f seedling trees th at have never
been topworiced to scions.

398
 A. P . D . MCCLEAN A ND A. H . P . ENGELBRECHT

M any o f the sweet oranges grafted on sweet orange stocks show ed a fine fluting
of the inner faces of wood and bark, rath er sim ilar to that illustrated by D u Charm e
& K n o rr (1954).
The existence of vascular projections and pits away from the line o f the union
are recorded for completeness of the sym ptom picture in the trunks o f citrus trees
and not necessarily because they are considered to be associated with abnorm al
bud-unions. Tristeza virus is w idespread and probably universal in South A frican
citrus trees, and there is evidence th at xyloporosis virus occurs in the clonal progeny
of some varieties. Both these viruses can induce vascular projections and pits. And
there may be others, still to be identified, with the same properties.
Reference has already been m ade above to the belief in Florida th at xyloporosis
(cachexia) m ay be the prim ary cause o f the abnorm al unions between sweet oranges
and rough lemon. Two pieces o f evidence from our work suggest th at this may not
be the case. In the transm ission tests to seedlings o f O rlando tangelo a variety o f
sweet orange (Pickstone Navel) w ith bud-union sym ptom s has failed so far to give
a reaction for xyloporosis (cachexia). A nd the strain of Valencia used in rootstock
and other field experim ents at N elspruit m akes a norm al union with rough lemon
(Plate III, Fig. 6), yet its behaviour on sweet lime stocks strongly suggests th at the
p arent tree is infected with xyloporosis. We are, therefore, not yet convinced th at
the bud-union sym ptom is an indicator for xyloporosis (cachexia) virus. F urther
experim ents seem necessary to establish the point, and observations are especialy
needed on the behaviour o f trees o f sweet orange on rough lemon into which
xyloporosis has been introduced artificially, and a com parison made between them
and trees left free of infection.
If trees on rough lemon are harm ed because of the abnorm al changes at the
union, the dam age is slight. N o disease condition has been observed in such trees
com parable to the stunting and decline that occur in trees on stocks like the sour
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

orange, sweet lime, and trifoliate orange, when infected with certain viruses. In
spite o f the collar o f corky tissue round the trunk, and the presence o f only a few
layers o f functional phloem between stock and scion affected trees grow well, are
productive, and develop into trees o f good size. This applies not only to the
W ashington N avel and V alencia, but also to varieties like Sham outi and Tom ango.
M arloth (1957) records a better yield and better appearance of T om ango trees on
sweet orange stocks as com pared with the ones on rough lemon after the trees came
into full bearing. But there is no evidence yet th at this has anything to do with
xyloporosis or with the possible effect o f either this or some other virus in causing
abnorm al changes at the union o f trees on rough lemon stocks.
In the variety collection at N elspruit m ost sweet oranges are represented by
two adjacent trees, the one on sweet orange stock, the other on rough lemon. The
trees of each pair are mostly of the same age. A few of them are seven to ten years
old and the rem ainder from 10 to 23 years old. As m entioned above som e o f the
varieties form a norm al union with rough lemon and others an abnorm al one. This
collection o f trees thus afforded an o p portunity o f seeing w hether the type o f union
form ed with rough lemon has any influence on the com parative perform ance of
the varieties on the two rootstocks, rough lemon and sweet orange. All com parisons
were m ade between the two trees of a pair. To assist in deciding which tree in each
pair had m ade the better grow th, as this was not always possible by
visual exam ination we m easured the volume * occupied by the foliage of each tree.
* T he volum e was calculated from the form ula jr’(0 ' 0 8 x h) — (0-004 x x), x being the
circum ference o f the foliage o f the tree and h the height from the po in t o f the lowest branches to
the to p o f the tree. T he form ula was suggested by M r. W . Langenegger and M r. W. B asson o f the
Research Station, N elspruit, and is based on the volum e o f a cylinder plu s th a t o f h alf a sphere.

399
 XYLOPOROSIS, CACHEXIA AND ABNORMAL B U D -U N IO N S IN SOUTH AFRICAN CITRUS TREES

It is not claim ed that the figures calculated by this form ula represent an accurate
measure o f tree volume. They merely give an index o f tree size, and provide a
basis for com paring the size o f two trees. The difference in volum e between the two
trees o f a pair varied from a few cubic feet to m ore than 1,500 cubic feet. In one
extreme case the difference was m ore than 3,000 cubic feet. Jn extreme cases like
this the difference in size betw een trees was striking to the eye. Only trees of
the same age were com pared. Based on the volume determ inations our estim ate o f
the relative grow th perform ances o f the trees on the two stocks in relation to the
type o f bud-union with rough lem on is sum m arised as follow s:—
(a) O f the varieties form ing norm al unions with rough lemon, the trees o f
22 had a larger foliage volum e on sweet stock than on rough lemon. The
reverse was true for nine others, and two showed no difference.
( b) O f the varieties form ing abnorm al unions with rough lem on, the trees
o f eight had a larger foliage volum e on sweet stock than on rough lemon.
The reverse was true for nine others and two showed no difference.
A lthough the figures show m ore varieties perform ing better on sweet oranges
than on rough lem on, there is no evidence th at this is in any way correlated with the
type of bud-union between the scion varieties and rough lemon. W e are still far
from know ing from the available inform ation w hat effects, if any, xyloporosis or
any other virus has in determ ining which is the better stock for sweet oranges, the
rough lemon or the sweet orange itself.

Citrus trees on sto ck s o f Calamondin and som e Kumquat hybrids

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

A sim ilar bud-union abnorm ality to the one above is described from Texas by
Olson (1954) in experim ental trees on rootstocks o f C alam ondin and some K um quat
hybrids. The sym ptom s follow much the same p attern : a constriction encircling
the w ood, a projection from the bark, and some gum im pregnation o f the inner
phloem in the neighbourhood o f the union. The condition was observed in trees
o f two varieties o f grapefruit (Shary red, and W ebb red blush) and in Valencia orange.
All the scions are noted as carrying xyloporosis (cachexia) though this virus
was not necessarily held to be the cause o f the abnorm al unions.
A t the N elspruit S tation are three trees o f Nagam i k u m quat which are budded
on seedling stocks o f N agam i kum quat. All o f them have an abnorm al union with a
ridge projecting from the face o f the bark and a groove encircling the wood. The
trees after 16 years are in poor condition.

Citrus trees on sto ck s o f trifoliate orange and trifoliate hybrids

In C alifornia W eathers, C alavan, W allace, & Christiansen (1955) report that

E ureka lem on trees on T royer citrange rootstocks show a severe bud-union disorder
after grow ing well for three years. In addition to extensive bark and w ood necrosis
o f the rootstock, affected trees show a narrow d ark brow n line in the cam bial faces
o f the bark and w ood along the line o f the union. This occurred in trees form ed
from b o th old clonal lines o f Eureka lemon and from new nucellar ones. It occurred
also when the same scions were p u t on trifoliate stocks. A ll strains o f Lisbon lemon
on the other hand, have continued to grow norm ally on these stocks.

400
 A. P. D. MCCLEAN AND A. H. P . ENGELBRECHT

G ra n t e t al. (1957) in Brazil also record an abnorm al union betw een E ureka
lem on and trifoliate stock. They describe an indentation in the w ood and bark
cracking, sym ptom s which they think are essentially the same as those reported by
W eathers et al. (1955).

This trouble is also thought to be due to virus infection, but as yet unidentified.

In rootstock experim ents at N elspruit all trees o f sweet orange (W ashington

N avel, T om ango and H am lin) on trifoliate stocks with exocortis th at have been
exam ined have shown a ridge from the inner face o f the b ark and a constriction in the
w ood along the line o f the union (Plate IV, Fig. 3), similar to those associated w ith
the abnorm al union between sweet orange and rough lemon. It is not know n w hether
this is a p a rt of the sym ptom picture o f exocortis in these trees. All sweet oranges
w ithout exocortis (Valencia, Pretoria Navel, D u Roi and De W ildt) have norm al
unions on trifoliate orange.

O f other scion varieties in the collection at the N elspruit Station known to be

free o f exocortis Em press m andarin, M inneola tangelo and W est Indian lime also
have norm al unions on trifoliate orange, but N atal naartje and kum quat show some
tooth-like projections from the bark an d gum pockets along the union. Rex grape­
fruit (thought to be a grapefruit hybrid o f local origin), also free of exocortis’, shows a
series o f short corrugations across the line o f the union on the cam bial faces o f both
b a rk and wood and gum pockets in the bark. The tree is po o r and in a state of
decline and its m ost striking abnorm ality is the abundance o f m edullary ray
projections from the w ood o f the scion thro u g h o u t the tru n k and branches.
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

A m ongst the trees form ed from scions o f seedling origin on trifoliate stocks
in the orchard at o u r Buffelspoort S tation are two examples showing a bud union
projection and constriction, and neither is infected with exocortis. The first one is a
sexual variant o f M arsh grapefruit and is readily distinguished from the p arent type
by the general appearance o f its foliage “and the coarse dry flesh o f its fruits. We
have five sister trees: two on rough lem on stocks, one on sour orange, and two
on trifoliate orange. The trees on rough lem on and sour orange are in good condition.
The unions are norm al, but the scion p art o f the tru nks all show, away from the union,
ridge-like projections from the b ark and corresponding trough-like depressions in
the w ood. Similar vascular abnorm alities also occur in the rough lem on stocks but
not in the sour stock. The two trees on trifoliate orange are dwarfed, have yellowish
leaves, and are in a com paratively p oor condition. B oth have an abnorm al union
w ith a prom inent ridge projecting from the inner face o f the b ark and fitting into a
deep groove encircling the w ood (Plate IV, Fig. 1).

The other sexual variant is a seedling o f W ashington Navel, differing widely in

foliage and fruit characters from b o th the W ashington Navel itself and sweet oranges
generally. O f six sister trees, tw o are on rough lemon and four on trifoliate orange.
AH the trees show m arked pitting th ro u g h o u t their trunks and branches and have
given a positive reaction for tristeza virus by inoculation to seedlings o f W est Indian
lime. The tw o on rough lem on have norm al unions, and the four on trifoliate orange
abnorm al ones. The ridge on the inner face o f the b ark is very narrow w ith a
corresponding shallow ring, yellowish in colour, in the wood. In one tree the
abnorm ality continues right round the tru n k and in the others only p art o f the way
(Plate IV, Fig. 2).
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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BU D -U N IO N S TN SOUTH AFRICAN CITRUS TREES

In the same orchard as the two variants are trees on trifoliate stocks whose
scions are from “ true-to-type ” seedlings o f W ashington Navel and M arsh grape­
fruit. All these trees have norm al unions as do also their sister trees on rough lemon
stocks. In each case the variant and the “ good-type ” seedlings o f the same variety
came from seed o f the same parent.

All the trees referred to in the orchard at Buffelspoort were planted in the field
w ithout inoculation and were left to pick up naturally any infection carried by
aphides ( T oxoptera citriciclus).

The cause o f the abnorm al unions in the various trees on trifoliate stock is not
know n. T here is no evidence that they are related to those associated with sweet
oranges on rough lemon, and in fact there is still no evidence to show they themselves
are related.

Summ ary

1. In rootstock experim ents a t N elspruit the behaviour o f m ost scions on stocks

o f sweet lime is poor. Two viruses could be responsible: tristeza and xyloporosis.
Tristeza is w idespread and m ay be universal in South A frican citrus trees and
probably has contributed partly or wholly to the po o r condition o f the trees. But
the extreme dwarfing and unhealthy condition o f the trees o f some scions, and the
type o f vascular pits and projections present in the sweet lime stocks suggest th at
they m ay be infected in addition with xyloporosis. This applies m ore especially to
Valencia, W ashington Navel, Tom ango orange, M arsh grapefruit and L isbon lem on.
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

P ro o f th at xyloporosis (cachexia) does indeed occur in some scions comes from

an experim ent in which seedlings o f O rlando tangelo and M inneola tangelo were
inoculated from different orchard trees. The test was positive from two sources:
the Lisbon lemon in the N elspruit collection and a E ureka lemon growing in a private
orchard.

2. The trees on rough lem on stocks o f m any varieties o f sweet oranges in the
collection at N elspruit show an abnorm al bud-union similar to the ones described
from F lo rid a and Israel. The same trouble was observed in both W ashington Navel
and Valencia in the orchards o f two private estates. The health o f affected trees
does not seem to be affected adversely. The condition is peculiar to trees on rough
lemon an d has not been observed in any trees on stocks o f sweet orange. Some
evidence is given th a t throw s d o u b t on the suggestion th a t the condition is caused by
xyloporosis (cachexia).

B ud-union disorders o f m uch the same pattern are described in trees o f some
scions on trifoliate stocks. Trees to show them include those form ed from the scions
o f sweet oranges infected with exocortis an d those from two scions o f seedling origin
th at are free o f exocortis. The two seedling scions are sexual variants, the one o f
M arsh grapefruit an d the other o f W ashington Navel. There is no evidence that
these disorders are related to those of sweet oranges or rough lem on, or for th at
m atter th at they themselves are related.

A bud-union d iso rd er o f a tree o f N agam i kum quat on a stock o f N agam i

kum quat is also recorded.

402
 A. P . D . MCCLEAN AND A. H . P . ENGELBRECHT

Opsomming
X IL O P O R O SIS , K A C H E K S IE E N A B N O R M A L E E N T V E R B IN D IN G S
I N S U ID -A F R IK A A N S E S 1 T R U S B 0 M E
1. D ie m eerderheid van die bostam m e g roei sw ak op soetlem m etjie-onderstam m e,
in die onderstam proewe te N elspruit. Twee virusse, nl. tristeza en xiloporosis, kan
hiervoor verantwoordelik wees. T risteza is w yd verspreid en w aarskynlik algemeen in
Suid-A frika, en is w aarskynlik gedeeltelik o f heeltem al verantwoordelik vir die sw ak
toestand van die borne. D ie uiterm atige verdwerging en siek lik e toestand van die bostam ­
m e tesam e m et die tipe van gleuwe en u itsteeksels in die flo eem en xileem van die soet-
lem m etjie-onderstam m e in som m ige borne, wek die vermoede d at die bom e ook m et
xiloporosis besm et is. D it g eld veral by Valencia, Washingtonnawel, Tomangolemoen,
M arsh se pom elo en Lissabonsuurlemoen.
D ie bew ys dat xiloporosis (kacheksie ) wei voorkom in som m ige van die bostam m e,
blyk uit ’n p r o e f waar ogies van ander bom e oorgeent is op O rlando-tangelo en M inneola-
tangelosaailinge. Twee van die oorentings, nl. die Lissabonsuurlemoen in die N elspruit-
versameling en ’n Eurekasuurlemoen vanuit ’n private boord het positiew e reaksies
getoon.
2. Abnorm ale entverbindings, soos b esk ryj in Florida en Israel, kom voor by
bom e van ’n hele aantal varieteite op growweskilsuurlem oenonderstam m e, in die
versameling te N elspruit. D ieselfde abnorm aliteit is opgem erk by Washingtonnawel
en Valencia op growweskilsuurlemoen, in die boorde van tw ee p riva te landgoedere.
D ie gesondheid van die bom e is egter blykbaar nie ernstig be'invloed nie. H ierdie
toestand is eie aan bom e op growweskilsuurlem oenonderstam m e en is nie waargeneem
by bom e op soetlem oenonderstam m e nie. Bewyse word aangevoer wat tw yfel laat ont-
staan oor die bewering, d a t d it deur xiloporosis ( kacheksie) veroorsaak word.
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

Entverbindings wat min or m eer hierm ee ooreenstem , word b e s k ry f by sekere

bostam m e op Trifoliata-onderstam m e. H ierdie abnorm aliteit kom voor by bom e wat
bestaan uit bostam m e van soetlem oene w at besm et is m et exocortis en ook by twee
bostam m e, vry van exocortis, en van saailing oorsprong. D ie tw ee bostam m e is
geslaglelike variante. Die een is van M arsh se pom elo en die ander van Washington­
nawel. D aar is geen bew ys dat hierdie abnorm aliteite verband hou m et d ie van soet-
lemoen o f grow weskilsuurlem oen , o f selfs dat dit onderlinge verband het nie.
'n Entverbindingabnorm aliteit van die entverbinding by 'n N agam i-kum kwatboom
op ’n onderstam van N agam i-kum kw at is ook aangemeld.

R esum e
X Y L O P O R O S I S , C A C H E X IA E T D E S S O U D U R E S A N O R M A L E S D E
G REFFES E N E C U S S O N S U R L E S A G R U M E S S U D -A F R IC A IN E S
1. D ans les experiences a N elspruit avec des souches, le com portem ent de la
plu part des greffons sur souches de lim e douce est decourageant. II est possible que
deux virus sont responsables, a savoir: tristesse et xyloporosis. Tristesse est tres
freq u en te et p eu t etre universelle dans les agrumes sud-africaines et, tres probablem ent,
a contribue en p a rt ou en to ta l a la condition deplorable des arbres. M ais le nainisme
extrem e et la condition malsaine des arbres de quelque greffons, et le type de fa v e o le s
vasculaires et projections presen ts dans les souches de lime douce indiquent qu’ils
peuvent aussi etre attein ts de xyloporosis. C eci est applicable plus particulierem ent
aux Valencia, Washington navel, orange Tomango, pam plem ousse M arsh et au
limon Lisbonne.

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BUD -U N IO N S IN SOUTH AFRICAN CITRUS TREES

L a preuve que xyloporosis (cachexia ) est recontree en effet dans quelques greffons
est fournie p a r une experience dans laquelle des jeun es plan tes de tangelo Orlando et de
tangelo M inneola fu ren t inoculees avec des ecussons d ’arbres de differents vergers.
L ’experience etait positive de deux sources: le limon Lisbonne de la col.ection de
N elspruit et un limon Eureka d ’un verger p rive.
2. L e s arbres, sur souches de limon rugueux, d ’orange douces de la collection de
N elspruit m ontrent une soudure anormale de la greffe en ecusson com m e dans des cas
d ec rits en Floride et en Israel. L a m em e difficulte f u t observee avec des W ashington
navel et Valencia dans les vergers de deux dom aines prives. II ne sem ble p a s que la
san te des arbres attein ts est affectee d'une m aniere adverse. C ette condition est
particu liere aux arbres su souche de limon rugueux e t n ’a p a s e te observee dans un
seul arbre sur souche d ’orange douce. II y a des in dicationsjetant la doute sur la sugges­
tion que cette condition est causee p a r xyloporosis (cachexia).
D es soudures anorm ales de greffes en ecusson de, pratiquem ent, la m em e nature
sont decrites dans les cas de quelques greffons sur des souches trifoliees, p a r exam ple,
des greffons d ’orange douce attein ts d ’exocortis et deux greffons d ’origine sauvageonne,
libre d'exocortis. L es deux greffons d ’origine sauvageonne sont des variantes sexuelles,
I’Une de pam plem ousse M arsh et I’autre de W ashtington navel. II n ’y a p a s d ’indications
qUe ces desordres ayent des rapports avec les desordres des oranges douces ou des
limons rugueux ou qu’elles soyent apparentees entre eux.
/
On a rencontre aussi une soudure anorm ale de greffe en ecusson d ’un arbre
N agam i kum quat sur souche de N agam i kumquat.

A cknow ledgem ents

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

We wish to record our thanks to D r. M arlo th fo r the facilities accorded us for

observations in the orchards o f the N elspruit S tation. W e also wish to th an k the
C rocodile Valley C itrus Estates an d Zebediela C itrus Estates for allow ing us to m ake
observations in their orchards.

R eferences

C A L A V A N , E. C. (1957). W ood pocket disease o f lem ons and seedless limes. Calif. C itrogr.
42, 300-304.
C H IL D S , J. F . L. (1950). T he cachexia disease o f O rlando tangelo. P la n t D is. R e p tr. 34, 295-298.
C H IL D S , J. F . L. (1951). C achexia, a bud transm itted disease a n d the m anifestation o f phloem
sym ptom s in certain varieties o f citrus, citrus relatives a n d hybrids. Proc. Fla. S tate H o rt.
Soc. 64, 47-51.
C H IL D S , J. F . L. (1952). C achexia disease, its bud transm ission a n d relation to xyloporosis a n d to
tristeza. P hytopath. 42, 265-268.
C H IL D S , J. F . L., G R IM M , G . R ., G R A N T , T. J., K N O R R , L. C. & N O R M A N , G . (1955). The
incidence o f xyloporosis (cachexia) in certain Florida citrus varieties. Proc. Fla. State H o rt.
Soc. 68, 77-82.
C H IL D S , J. F. L. (1956). T ransm ission experim ents and xyloporosis—cachexia relations in F lo rid a.
P la n t D is. R e p tr. 40, 143-145.
D U C H A R M E , E. P. (1951). X yloporosis o f citrus. Proc. Fla. State H o rt. Soc. 64, 57-60.
D U C H A R M E , E. P. & K N O R R , L. C. (1954). V ascular pits and pegs associated w ith diseases
in citrus. P lan t D is. R ep tr. 38, 127-142.
G R A N T , T. J., C O STA , A. S. & M O R E IR A , S. (1951). Tristeza disease o f citrus in Brazil. Calif.
C itrogr. 36, 310.
G R A N T , T. J., M O R E IR A , S. & C O STA , A . S. (1957). O bservations on ab n o rm al citrus rootstock
reactions in Brazil. P lan t D is. R eptr. 41, 743-748.

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G R IM M , G . R ., G R A N T , T. J. & C H IL D S , J. F . L. (1955). A bud-union abnorm ality o f rough

lem on ro o tsto ck w ith sweet orange scions. P lan t D is. R eptr. 39, 810-811.
M c C L E A N , A . P. D . (1950a). Possible identity o f three citrus diseases. N atu re, 164, 880.
M c C L E A N , A . P. D . (19506). Virus infections o f citrus in South A frica, iii. Stem -pitting disease
o f grapefruit. Frm g. in S. A fr. 25, 289-296.
M A R L O T H , R . H . (1938). T he citrus rootstock problem . Frm g. in S. Afr. 13, 226-231.
M A R L O T H , R . H . (1957). R ootstocks for Jaffa and Jo p p a oranges. J. H o rt. Sci. 32, 162-171.
M A R L O T H , R . H . (1958). R ootstocks fo r grapefruit. S. A fr. J. A gr. Sci. 1, 43-65.
M E N D E L , K . (1956). R ootstock-scion relationships in S ham outi trees on light soil. K tavim 6,
35-60. (English ed.)
O L SO N , E. O. (1954). Some b a rk a n d bud-union disorders o f m andarin and m andarin hybrid
rootstocks in Texas citrus plantings. A m er. Soc. H o rt. Sci. 63, 131-136.
O L SO N , E. O. & S H U L L , A . V. (1956). E xocortis a n d xyloporosis— budtransm ission virus diseases
o f R a n g p u r lim e and o th er m andarin-lim e rootstocks. P lan t D is. R eptr. 40, 939-946.
O P P E N H E IM E R , H . J. (1940). T he stock p roblem o f the Sham outi orange. H a d ar, 13, 245-248.
R E IC H E R T , I. & P E R L E B E R G E R , J. (1934). X yloporosis—the new citrus disease. H a d ar,
7. 163.
R E IC H E R T , I., Y O F F E , I. & B E N T A L , A . (1953). Sham outi orange o n various rootstocks and
its relation to xyloporosis. Palestine J. B ot. (R ehovot series) 8, 163-184.
W E A T H E R S , L. G ., C A L A V A N , E. C., W A L L A C E , J. M . & C H R IS T IA N S E N , D . W . (1955).
A bud-union and rootstock disorder o f T royer citrange with E ureka tops. P lan t D is. R eptr.
39, 665-669.
W IN O C O U R , E. (1956). T he anatom y a n d histology o f healthy a n d xyloporosis affected Palestine
sweet lim e rootstocks budded to S ham outi sweet orange. Bull. Res. C ounc. o f Israel D . B ot.
5D , 125-142.
Y E D ID Y A H , S. (1937). C itrus growing, (H ebrew ). 2nd ed., Tel Aviv.
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BU D -U N IO N S IN SOUTH AFRICAN CITRUS TREES

PL A T E I.— C itrus trees on sw eet lime stocks

PL A A T I.— Sitrusbome op soetlemmetjieonderstamme

F ig . 1. — V alencia, 13 years old show ing severe stunting a n d decline

F ig . 2. — L isbon lem on w ith flap o f b a rk rem oved to show num erous sm all pits and two
. longitudinal cracks in w ood o f sw eet lim e stock
F ig . 3. — Valencia— strip o f b a rk from tru n k across the union to show a longitudinal
crack in its o uter face
F i g . 4. — E m press m andarin—strip o f b a rk to show pinholing in its inner face on b o th
sides o f union, a n d som e ridge projections from the stock side
F ig . 5,,— Pretoria N avel— strip o f b a rk show ing p rom inent ridge-like projections from
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

the stock side.

F ig . 1..— Dertienjaaroue Valencia wat strawwe verdwerging en agteruitgang toon

F ig . 2 ■— Lissabonsuurlemoen, waarvan ’n strook bas verwyder is om die groot aantal klein
gleuwe en twee barste in die hont van die soetlemmetjieonderstam te toon
F ig . 3 ■— Valencia— 'n strook bas van die stain by die entverbinding wat ’« oorlangse bars
aan die buitekant vertoon
F ig . 4 .— Empress-nartjie— ’n strook bas m et gaatjies aan die binnekant van die bas aan
beide kante van die entverbinding, en m et rifagtige punte in die onderstamgedeelte
F ig . 5,.— Pretorianawel— strook bas m et duidelike rifagtige nitsteeksels

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P L A T E II.— O rla n d o tan g elo sh o w in g sy m p to m s o f x y lo p o ro sis (cachexia)

PLA A T II.— Orlanclo-langelo met simptome van xi/oporosis (kacheksie)

F jg . 1.— T ru n k o f seedling o n ro u g h lem o n sto c k w ith o u te r lay er o f b a rk p ared aw ay to

sh o w b ro w n sta in in g o f th e in n e r layers o n scion side a n d ab sen ce o f it o n th e
sto c k side
F ig . 2.— S am e tru n k w ith b a rk peeled aw ay to sh o w d isc o lo ra tio n and a b n o rm a l
a p p e a ra n c e o f w o o d an d in n er face o f the b a rk
F ig . 3.— C ro ss sectio n o f tr u n k sh o w in g g u m p o ck ets a lo n g in n er rin g o f th e w o o d , an d
b ro a d , lig h t-co lo u red m e d u lla ry rays ra d ia tin g from th e rin g to th e p e rip h e ry
F ig . 4.— A piece o f b a rk p rise d aw ay fro m th e w o o d to sh o w a c o u p le o f “ p eg ” p ro je c tio n s
fro m its in n er face, an d b ro a d m e d u llary rays an d g u m p o c k e ts in th e w ood
F ig . 5.— C ro ss sectio n , sh o w in g b ro a d m e d u lla ry rays p ro je c tin g from the su rface o f
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

the w o o d

F ig . I .— Siam van ’n saailing op growweskilsuurlemoen waarvan die b ’u itenste !ae van die bas
weggesny is om die bruin verkieuring van die binnesle !ae by die bostam en die
afwesigheid daarvan by die onderstam, te toon
F ig . 2.— Dieselfde slam met die bas opsy gelrek om die verkieuring en die abnormale
voorkoms van die hont en die binnekant van die bas te toon
F ig . 3.— ’n Dwarssnee van die slam wat die gomholles in die binnesle hont ring en die bree
liggektenrde vaalstrale toon, wat straalgewys van die ring uilloop
F ig . 4.— ’n D ee/ van die bas opsygetrek om 'n paar pnnlige nilsleeksels aan die binnekant
en bree vaalstrale en gomholles in die hont te toon
F ig . 5.— ’n Dwarsnee om die bree vaalstrale aan te toon wat bo die oppervlakte van die
hont nitsteek

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PL A T E III.— S w eet o ra n g e s o n ro u g h lem o n sto c k

PL A A T III.— Soetlemoene op growweskilsintrlemoenonderstamme

F ig . 1.— V alen cia 30 y ears o ld — tr u n k sh o w in g a p ro m in e n t c o rk y c o lla r a lo n g line o f

th e u n ion
F ig . 2.— M a ltese b lo o d o ra n g e sh o w in g a sim ila r a b n o rm a lity at the u n io n
F ig . 3.— W a sh in g to n N a v e l— lo n g itu d in a l se ctio n s th ro u g h b a rk ac ro ss u n io n to show
in tern al g u m pocket
F ig . 4.— W a sh in g to n N a v e l, w ith flap o f b a rk ac ro ss u n io n tied b ack to sh o w in tern al
to o th e d p ro je c tio n fro m in n er face o f th e b a rk a n d a c o rre s p o n d in g gro o v e
ro u n d th e w o o d
F ig . 5.— V alencia (ex p riv a te o rc h a rd )— strip o f b a rk fro m tru n k to sh o w n o rm a l u n io n
a n d m an y sm all rid g e p ro je c tio n s fro m th e sto c k side
Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

F ig . 6.— V alen cia (ex N e ls p ru it S ta tio n )— strip o f b a rk to sh o w n o rm a l u n io n a n d sm o o th

c a m b ia l face

F ig . 1.— Valencia, 30 jaar oitd—slam toon ’« dnidelike kiirkaglige rif by die entverbinding
F ig . 2.— ’n „ M altese ” bloedlemoen met ’n soorlgelyke abnormaliteit by die entverbinding
F ig . 3.— Washingtonnawel— lengtesnitte van die bas oor die entverbinding om die inwendige
gomholles le loon
F ig . 4. — Washingtonnawel me! ’n strook bas oor die entverbinding opsy getrek om die
getande uitsteeksel aan die binnekant van die bas, en ooreenstemmende g ro ef in
die hont te toon
F ig . 5.— Valencia (nit 'n private boord) — ’n strook bas met ’n nonnale entverbinding, en 'n
groot aantal rifagtige uitsteeksels by die onderstam
F i g . 6 .— Valencia (Nelspruitnavorsingstasie)— ’n strook bas met nonnale entverbinding
en met ’n gladde kambiale oppervlakte

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 XYLOPOROSIS, CACHEXIA AND ABNORMAL BUD-UNIONS IN SOUTH AFRICAN CITRUS TREES

PL A T E IV.— C itrus trees on trifoliate stocks with abnorm al bud-unions (ridge from face
o f bark and a groove in the wood)
PL A A T IV.— Sitrusbome op trifoliata-onderstamme met abnorntale entverbindings (’« r if
aan die binnesle oppervlakle van die bas en 'n g ro e f in die houl)

F ig . I.— M a rsh seedling 633 (sexual v a ria n t)— free o f ex o co rtis

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2012.)

F ig . 2. — W ashington Navel seedling 639 (sexual variant)— free o f exocortis

Fig. 3. — M editerranean Sweet (in collection o f N elspruit Station) with exocortis
F ig . I.— Marshpomelosaailing 633 (geslaglelike variant)— vry van exocortis
F ig . 2.— Washingtoimawelsaailing 639 (geslaglelike variant)— vry van exocortis
F ig . 3.— Mediterreense soetlemoen (in die Nelspruitversameling)—met exocortis

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