Cider Musings

Graft Incompatability in apples and pears.

After a talk I gave on the history of cider which mentioned grafting, I was asked a question, why do grafts in humans fail but not in apples. 

I was stumped at the time by this seemingly simple question but after reflection, it is of course a false equivalency argument.  

The mechanism of rejection of ‘foreign’ which evolutionary derived from defence from pathogens is mediated by entirely different mechanisms that have evolved in the plant and animal kingdoms since plants separated from the mainstream of eukaryotic cells by engulfing bacteria that evolved into chloroplasts. 

Both plants and animals reject foreign but over different timescales and different mechanisms. Animals with a rapid blood circulation, respond in minutes and hours, plants with a slower flow of sap in days and weeks. 

Grafting is an ancient horticultural practice for asexual plant propagation that joins the rootstock of one plant to the scion (a short segment of the desired budwood). There are records of this being applied in fruit tree propagation date back to 1560 BC in China, and the Greek and Roman times in the Mediterranean region. 

Grafting is a widely used for apple trees to propagate the favours of a particular type such as Granny Smith or Yarlington Mill, both chance finds. Each apple tree that grows from a pip is different from its parents and the range of desirable qualities for humans in apples is very limited. Much less than 1:1000. 

Graft failure in plants are due to entirely different mechanisms to mammals such as humans where the bone marrow and white blood cells, antibodies defend the body from infections and foreign material. 

In plants it appears not to be closely related to the mechanisms evolved to fight pathogens but rather from mechanisms around wound healing. 

It is not simple, many physiological, biochemical, molecular and gene changes occur from grafting that can influence the success of the graft ie its compatibility or non compatibility including insufficient genetic proximity, lignification at the graft union, poor graft architecture, insufficient cell recognition between union tissues, and metabolic differences in the scion and the rootstocks themselves.

As already referred to, molecular, biochemical, and physiological mechanisms that establish the graft union are those that heal tissue after wounding. Physically the thin cambium layer between, and giving rise to the phloem and xylem tissues that transport water minerals and sugars must line up and fuse correctly.  

The major events in a compatible graft union formation are firstly adhesion of the rootstock and scion, secondly the proliferation of callus cells to form a callus bridge, and thirdly vascular differentiation across the graft interface. The vascular connection between the scion and the rootstock is essential, or the scion will not resume growth successfully. 

The initiation of graft union formation is cell proliferation, and following the formation of a mass of pluripotent undifferentiated callus, vascular differentiation connects the phloem and xylem across the graft union. Too much lignin and the flow is interrupted, too little and the union break. Many factors can influence graft union success, including incompatibility (such as from virus, phytoplasma, other metabolic factors), polarity, the physical structure of the graft, environmental conditions, plant growth regulators, virus and fungal contamination.

Plant hormones, like auxin, ethylene (ET), cytokinin (CK), gibberellin (GA), and others orchestrate several crucial physiological and biochemical processes happening at the site of the graft union. Additionally, epigenetic changes at the union affect chromatin architecture by DNA methylation, histone modification, and the action of small RNA molecules. The mechanism triggering these effects likely is affected by hormonal crosstalk, protein and small molecules movement, nutrients uptake, and transport in the grafted trees. Plant hormones have discrete roles in establishing a successful graft union. For example, plant hormones mediate secretion of pectin to initiate adhesion between tissues, formation of de-differentiated callus cells, development of cellular junctions (plasmodesmata), initiation of cell division in the cambium, cortex and pith cells proximal to the phloem and xylem. Plant hormones, like auxin, ethylene (ET), cytokinin (CK), and gibberellin (GA) have interlinking roles in the regulation of several crucial physiological processes happening at the site of graft union

Auxin is probably the most important phytohormone for the formation of compatible graft unions. The formation of callus tissue depends on cell division proximal to vascular tissues, which is vital to the cellularisation of the graft union. During this developmental process, auxin as a morphogenic substance is released from vascular strands of the rootstock and the scion and induces the differentiation of vascular tissues, In addition, auxin promotes the expression of specific transcription factors that influence pith cell proliferation. Transcriptome analyses showed that a series of auxin response genes show changes in steady-state transcript accumulation during the grafting process. Auxin also cooperates with other hormones during graft union formation.

Ethylene is also involved in the wounding response and promotes cell expansion, callus formation, and cell proliferation. In addition, ethylene also regulates gene expression important for wound healing.

Cytokinins (CKs) can induce callus proliferation in the graft union during the process of wound healing. In addition, CKs can promote vascular cell growth, development of vascular bundles, and division of cambium tissue. Furthermore, CK regulates the expression of some key genes related to vascular tissue development. For instance, CKs regulated the activity of LONESOME HIGHWAY (LHW) gene ( isn’t that a great name!) that results in development of stele cells and formation of protoxylem. Gibberellins (GAs) have demonstrated roles in plant vascular growth, cambium activity, xylem expansion, and xylem fibre differentiation, as well as plant secondary growth. GA affects gene expression to facilitate the development of xylem tissue and stem growth. GA is mobile across the graft union and coordinates normal xylogenesis, formation of vascular bundles, as well as controlling cambium activity, xylem fibre differentiation, and reunion of cortex in the joining of scion and rootstock. So a complex process with multiple feedback loops.

Grafting between species within a genus is usually successful, so much wider than with mammals. Grafting in different genera within a same family is sometimes successful and used commercially as intergeneric grafting such as pear onto quince to dwarf the tree and speed up fruit production. This overcomes the problem elegantly encapsulated by this old West Country saying “Plant pears for your heirs”. I have grafted many Perry pear trees this way. and they start fruiting in 5-8 years rather than 15-20 years. However, the reverse combination of quince on pear rootstock is not compatible.  

The flow of secondary metabolites can play a role in graft incompatibility of fruit trees. However, this is only observed in some inter-generic combinations and is not a universal cause of graft failure. Prunasin is the most well-known example of a secondary metabolite and is involved in graft incompatibility in pear/quince combinations. Prunasin is a cyanogenic glycoside that that is present in quince rootstock and translocates into the pear scion phloem and is hydrolysed by a glucosidase. Subsequently, hydrocyanic acid (cyanide) is released, which causes cell death or damages xylem, and phloem at the graft interface! 

Macroscopically the incompatibility manifests in several ways . With apple this is often anatomic flaws leading to vascular discontinuity. In pear/quince pathogens such as phytoplasma lower lignification disruption of cambium and vascular flow, with death of the scion. Viruses can affect apple graft union eg. AUND ( Apple union and necrosis disease) is caused by tomato ringspot virus (TmRSV).

In some cases, graft incompatibility leads to a smooth break at the point of the graft union due to disruption in cambial and vascular continuity. These structural anomalies cause mechanical weakness of the union which may break after some years later or after strong winds as I have found. Some changes of localised incompatibility can be overcome with an interested of graft wood compatible with the rootstock and scion. Grafting of ‘Bartlett’ (‘Williams’) pear onto quince rootstock is an example of localised incompatibility that can change to a compatible three-graft combination using ‘Beurré Hardy’ pear as the interstem with satisfactory tree grow and strong unions.  

In other cases, the symptoms of incompatible graft combinations can develop yellow and red-coloured leaves, leaf curling, reddening of shoots, slow vegetative growth and early defoliation at the end of the growing season, premature death of the grafted trees, failure to produce vegetative growth, shoot die-back, and differences in growth rate of scion and rootstock causing disproportionate overgrowths above or below the graft union. This type of incompatibility is known as translocated incompatibility and it is seen with some flowering cherry trees around Wellington. These symptoms can occur within a number of days or emerge over years.

Graft incompatibility is fundamentally controlled by the genetics of the rootstock and scion. And this is probably the underlying cause of some rejections. Changes in the expression of genes encoding enzymes of metabolism are important in graft incompatibility. Two type PAL genes (ParPAL1 and ParPAL2) in Prunus spp., showed ParPAL1 was more highly expressed at 10 and 21 days after grafting, and ParPAL2 was more highly expressed at 21 days after grafting in failing grafts in comparison to compatible combinations and subsequently more polyphenols produced at incompatible graft.

So humans and plants are entirely different in the mechanisms of graft rejection. Such is the wonders of life. Understanding the mechanisms of graft rejection in plants is economically important in horticulture. Only recently has this been investigated. However prior to that horticulturists knew from experience which grafts worked empirically; the wisdom of the profession.