The Impact of Self-Incompatibility on Almond Pollination

Jun 28, 2023 | Almonds

By Gal Sapir

Self-incompatibility (SI) plays a crucial role in the pollination process of flowering plants by preventing fertilization with their own pollen. As a result, SI plants rely on cross-fertilization to produce fruit. Many plant species exhibit self-incompatibility, employing various mechanisms to prevent self-pollen from reaching the ovule. One extensively studied system is S-RNase-mediated gametophytic SI (GSI), in which the pollen grain is halted in the style if its S haplotype matches either of the S haplotypes present in the pistil (1).

Research into this system has revealed that pollen rejection in the style is governed by a haplotype-specific RNase called S-RNase (2). The Rosaceae family, which includes plants like roses, strawberries, pome fruits (apples, quinces, pears), and stone fruits (almonds, apricots, cherries, peaches, plums), features S-RNase. Genetic analysis has identified the GSI system as a single locus known as the S-locus. In GSI, S-RNases are already present in the lumen of the pistil when the flower opens. Upon landing on the stigma, a pollen grain begins to germinate into the pistil, allowing the S-RNases to enter the pollen tube regardless of its haplotype (3). In the pollen tube, nonself-S-RNases are tagged by SLF/SFB and subsequently degraded through the ubiquitin/proteasome pathway, while the self-S-RNase remains protected from degradation. Consequently, only self-S-RNase triggers RNA degradation in the pollen (4), leading to growth inhibition and self-incompatibility.

From Field Experiments to Molecular Analysis

Most cultivars of Rosaceous fruits exhibit self-incompatibility, necessitating the presence of at least two compatible cultivars in orchards. Traditionally, compatibility was determined through field experiments involving natural and hand-pollination of cultivar pairs. However, this method is prone to inaccuracies due to the influence of agrotechnical and environmental factors on fruit-set levels. Determining varying levels of compatibility is particularly challenging using this approach. Moreover, this methodology is time-consuming and labor-intensive as it requires multiple seasons to obtain reliable data. Consequently, a more accurate and simple molecular-based analysis has replaced this method.

The development of molecular-based analysis became feasible when it was discovered that each S-RNase allele represents a specific S-locus haplotype. Since the identification of the first Rosaceae S-RNase in Japanese pear by Sassa et al. (5), numerous S-RNase alleles from economically important fruit-producing Rosaceae species have been molecularly identified. The PCR-based method has been the primary molecular technique developed for this purpose, and it has become the preferred approach once numerous S-RNase alleles were cloned.

Almond Pollination: Decoding S-Alleles and Compatibility Groups

In the case of almonds, as with other Rosaceae species, the process of S-RNase genotyping starts with controlled crosses (6). This is followed by utilizing differences in the isoelectric characteristics of the stylar proteins (7), and ultimately using consensus primers from another Prunus species (8), which is highly efficient in the case of almonds. Several researchers from different labs and countries have worked in parallel, resulting in the S-genotyping of all cultivated almond varieties, albeit with some overlaps and differences in the results. Gomez et al. (2019) (9) organized and revised the available data to publish a comprehensive table of almond S-alleles categorized by compatibility groups. Growers use these tables in combination with other factors, particularly flowering overlap.

The Impact of Semi-Compatibility on Pollination Efficiency in Rosaceous Species

It is important to note that cultivars from different Cross Incompatibility Groups (CIG) can share the same S-allele, a phenomenon that is sometimes overlooked. This division of cultivars into what is known as “semi-compatible” implies that half of their pollen grains cannot fertilize and are rejected by semi-compatible stigma (pic 1).

graphic describing full compatability and semicompatability

Pic 1 – illustration of full-compatibility pollination vs. semi-compatibility

Field experiments conducted in various Rosaceae species have shown that the fertilization efficiency of semi-compatible pollinators is significantly lower compared to fully compatible ones (10-13). Researchers have suggested that the lower yields observed in semi-compatible cultivars could be attributed to pollen deficiency resulting from the rejection of half the pollen. They hypothesized that pollen deficiency becomes critical under sub-optimal pollination conditions, such as inclement weather (cloudiness, rain, and low temperatures) disrupting honeybee activity during the flowering period, as well as heatwaves during early fruit-set causing fruitlet drop (14). For example, Table 1 presents the differences in fruit set between semi and fully-compatible cultivars after natural open pollination in different Japanese plum varieties (13). Consequently, when planning to establish a new orchard, growers should exercise caution when selecting cultivars from different Cross Incompatibility Groups (CIG). Instead, the specific S-allele of each combination should be carefully considered.

Table 1 – The influence of compatibility on fruit-set

Sapir et al. (2008)

Conclusions

In conclusion, self-incompatibility plays a vital role in almond pollination and affects various aspects of fruit production. Understanding the molecular mechanisms behind self-incompatibility and employing molecular-based analysis methods enable growers to make informed decisions when selecting compatible cultivars. This knowledge, combined with considerations of flowering overlap and other factors, can contribute to maximizing fruit-set levels and optimizing orchard productivity.

References

(1) McCubbin, Andrew G., and Teh-hui Kao. “Molecular recognition and response in pollen and pistil interactions.” Annual review of cell and developmental biology 16.1 (2000): 333-364.‏

(2) Anderson, M. A., et al. “Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata.” Nature 321.6065 (1986): 38-44.‏

(3) Luu, Doan-Trung, et al. “S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility.” Nature 407.6804 (2000): 649-651.‏

(4) McClure, Bruce A., et al. “Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA.” Nature 347.6295 (1990): 757-760.‏

(5) Sassa, Hidenori, Hisashi Hirano, and Hiroshi Ikehashi. “Self-incompatibility-related RNases in styles of Japanese pear (Pyrus serotina Rehd.).” Plant and cell physiology 33.6 (1992): 811-814.‏

(6) Ballester, J., et al. “Location of the self‐incompatibility gene on the almond linkage map.” Plant Breeding 117.1 (1998): 69-72.‏

(7) Bosković, R., et al. “A stylar ribonuclease assay to detect self-compatible seedlings in almond progenies.” Theoretical and Applied Genetics 99 (1999): 800-810.‏

(8) Sutherland, B. G., et al. “Primers amplifying a range of Prunus S‐alleles.” Plant Breeding 123.6 (2004): 582-584.‏

(9) Gómez, Eva María, et al. “Cross-incompatibility in the cultivated almond (Prunus dulcis): Updating, revision and correction.” Scientia Horticulturae 245 (2019): 218-223.‏

(10) Goldway, Martin, et al. “Jonathan’ apple is a lower-potency pollenizer of ‘Topred’ than ‘Golden Delicious’ due to partial S-allele incompatibility.” The Journal of Horticultural Science and Biotechnology 74.3 (1999): 381-385.‏

(11) Schneider, Doron, Raphael A. Stern, and Martin Goldway. “A comparison between semi-and fully compatible apple pollinators grown under suboptimal pollination conditions.” HortScience 40.5 (2005): 1280-1282.‏

(12) Zisovich, Annat, et al. “Fertilisation efficiency of semi-and fully-compatible European pear (Pyrus communis L.) cultivars.” The Journal of Horticultural Science and Biotechnology 80.1 (2005): 143-146.‏

(13) Sapir, Gal, et al. “Full compatibility is superior to semi-compatibility for fruit set in Japanese plum (Prunus salicina Lindl.) cultivars.” Scientia horticulturae 116.4 (2008): 394-398.‏

(14)Stern, R. A., et al. “The appropriate management of honey bee colonies for pollination of Rosaceae fruit trees in warm climates.” Middle Eastern and Russian Journal of Plant Science and Biotechnology 1.1 (2007): 13-19.

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