Exploring the mysteries of sex . . . and taking control!

I’ve been fascinated with sex (especially controlled sex) since my undergraduate days at the University of Southampton between 1967 and 1970. We were the socially permissive flower power generation.

But before you get too excited about this post’s content, I need to point out that, as a former botany student, I’m referring to sex among plants! And plant breeding. The real flower power!

Joe Smartt and Edgar Anderson

I guess it all started with two final year honours course on plant speciation (how different species evolve) and plant breeding, taught by geneticist Dr Joe Smartt. It was through the first that I discovered the beauty of introgressive hybridization (a mechanism that blends the gene pools of separate species; see a diagrammatic explanation in this post), a concept first expounded by another of my botanical heroes, Dr Edgar Anderson. And, there was this transformative book to dip into: Variation and Evolution in Plants (published 1950) by another great American botanist, G Ledyard Stebbins. In Joe’s introduction to plant breeding, we followed yet another classic text: Principles of Plant Breeding by American plant breeder and geneticist, Robert W Allard.

Trevor Williams

And when I moved to the University of Birmingham as a graduate student in September 1970, to study for a Master’s degree in plant genetic resources, Trevor Williams taught a fascinating course on plant variation, emphasising their breeding systems, and how understanding of these was important for the conservation and use of genetic resources. Much of my career subsequently was then spent studying variation and breeding systems in two important crop species, potatoes and rice, and a minor legume species, the grasspea.

Plants reproduce in the most weird and wonderful ways. If they didn’t, humanity’s days would be numbered. Where would we be if wheat and rice plants failed to produce their grains, the potato its underground treasure of tubers, or the banana those abundant hands of green fruits? No wonder in times past folks celebrated a Harvest Festival each autumn to give thanks for a successful harvest.

Beautiful acorns on the pedunculate oak, Quercus robur

You only have to look about you in late summer, as I did each day on my walks last year, to see Nature’s bounty all around—the consequence of plant sex. The trees and bushes were dripping with fruit—2020 was a mast year (as I have written about before). I don’t think I’ve seen such a year for acorns on the oak trees. And the chestnuts, hazels, and so many others. Such exuberant fecundity!

Have you ever looked closely at a ‘typical’ flower? Well, for the most part you can see the female pistil(s) comprising the style, stigma, and ovary, and the male stamens that carry the pollen.

However, there are many variations on this basic theme, different arrangements of the sex organs, even separate male and female flowers on the same plant (known as monoecy; maize is a good example) or separate plants (dioecy; holly). Differences in plant reproductive morphology promote self fertilization or cross fertilization. In addition, there is a host of physical and genetic mechanisms to promote or prevent self fertilization, as well as limiting sex between different species. All of this is aimed at ensuring a next generation of plants, and the one after that, and so on.

Plants attract a host of pollinators: visiting insects such as bees and moths, even some nectar-feeding marsupials and bats. I watched a remarkable sequence on David Attenborough’s latest blockbuster series, A Perfect Planet a few nights ago, about the fascinating pollination role of fig wasps.

Then I came across this tweet. Cockroaches of all creatures!

Wind pollination is a common feature of many grasses. However, several wheat and rice species, for example, promiscuously dangle their stamens apparently seeking cross fertilization. But they have often self fertilized before their flowers open. That’s not to deny that some cross pollination does occur in these species, but it’s generally the exception.

Some plants appear to reproduce sexually, but they have got around actual sex through a mechanism known as apomixis. These plants produce seeds but not following the normal fertilization process, so each seedling is a genetic copy of the ‘mother’ plant.

Berries on a diploid potato species, Solanum berthaultii

Other species have given up sex (almost) altogether, instead reproducing vegetatively with the ‘offspring’ being genetically identical (or essentially identical) to the mother plant. In others, like the potato, propagation is primarily through tubers. Yet, in the Andes especially where potatoes were first domesticated, many varieties are extremely sexually fertile, and produce berries rather like small tomatoes, although they are inedible. They contain lots of small seeds that we often refer to as true potato seed or TPS. In fact, in one experiment I observed at the International Potato Center (CIP) in Peru where I worked during the 1970s, a colleague of mine recorded a particular variety known as Renacimiento producing more than 20 t/ha of berries, in addition to about 20 t of tubers.

Anyway, I digress somewhat. During the years I was active scientifically (before I joined the ranks of senior management at the International Rice Research Institute in the Philippines, IRRI in the Philippines), I looked into various aspects of reproductive biology of several species.

In my doctoral research, carried out in the Andes of Peru, I investigated the breeding relationships between potato varieties with different numbers of chromosomes. The potato we consume almost on a daily basis (at least in my home) is known scientifically as Solanum tuberosum, and has four sets (48 in total) of chromosomes. It is what we call a tetraploid. Many other potato species have only two sets or 24 chromosomes, and are known as diploids. The tetraploid forms are mostly self fertile; diploids, on the other hand, have a genetic system of self incompatibility, and will only produce seeds if pollinated with pollen from a different genetic type.

This or similar system of self incompatibility is known from other species, like poppies for example. Anyway, the outcome is that ‘self’ pollen will not germinate on the stigma. The two images below (of various pollinations among wild potatoes), show a typical compatible pollination and fertilization event. Lots of pollen grains have stuck to the stigma, have germinated and grown the length of the style to reach the numerous ovules in the ovary.

In these next images, showing incompatible pollinations, few pollen grains remain on the stigma, not all germinated, and those that did, grew erratically. A few pollen tubes may reach the ovules but compared to the compatible pollinations, they are many fewer.

In the 1970s, one of my colleagues at CIP, Chilean breeder/agronomist Primo Accatino, championed the use of TPS as an alternative to propagation from seed tubers. One of the weak links, as it were, in any potato production cycle is the availability and cost of disease-free seed tubers. So TPS was seen as potentially fulfilling a gap in many developing countries that had neither the infrastructure nor staff to support seed potato production.

As I mentioned earlier, the common potato is a tetraploid with four sets of chromosomes, and this complicates the genetics and breeding. Breeding at the diploid level could be more straightforward. At least that was the hope and the challenge when I embarked on a project to produce TPS lines through inbreeding diploid potatoes and single seed descent. Funded by the British government, it involved scientists at the University of Birmingham (where I had joined the staff in 1981), the former Plant Breeding Institute in Cambridge, and CIP in Peru.

Was this just a pipe dream? Perhaps. Before developing the project concept, I’d had extensive discussions with my colleague at Birmingham, geneticist Dr Mike Lawrence who worked on self incompatibility in poppies (that has a similar genetic system to that in potatoes). His experience with poppies showed that if one tried long and hard enough, it was possible to break the self incompatibility.

Flowers of Solanum chacoense

We tried—and ultimately failed—closing the project after five years. We decided it would take just too much investment to make progress. If only we’d had available then what are now helping to transform potato breeding: self compatible diploid lines. At the end of the 1990s, scientists working at the USDA potato collection in Sturgeon Bay, Wisconsin identified self compatible lines in the widespread wild species Solanum chacoense. The Sli gene that confers self compatibility is apparently more widespread than previously thought, and has now been bred into diploid lines. Had we had those self compatible lines back in the 1980s, our work would have perhaps have reached a better conclusion.

When I moved to the Philippines in 1991 to head IRRI’s Genetic Resources Center (GRC), I had a collection of around 100,000 different lines of rice, cultivated and wild, to conserve in the institute’s International Rice Genebank.

With my colleagues in GRC, Dr Lu Bao-Rong, Amita ‘Amy’ Juliano and Dr Ma Elizabeth ‘Yvette’ Naredo, I spent several years investigating the breeding relationships between the cultivated forms of rice, Oryza sativa from Asia, and O. glaberrima from West Africa, and the closest wild Oryza species with a similar AA genome. We made thousands of crosses with the aim of understanding not only the breeding relationships, which is important to be able to better use wild species in rice breeding, but also to understand the taxonomy of wild and cultivated rices.

Pollinations (L) in the genebank screenhouse among AA genome species from Asia, Australia, and the New World, and (R) a crossing polygon from those pollinations expressed in terms of spikelet fertility.

This work led to several scientific publications, which you can access here: just look for publications with our names.

Another aspect of plant sex, important for genebank managers, is how the environment can affect plant fertility. While the seeds of many species (including rice and potatoes) can be stored at a low temperature (typically -18ºC) and for decades if not longer, it is essential that only the best seeds are placed in a genebank for long term conservation. That means ensuring that the growing conditions are the best possible to produce seeds of high quality—and in abundance—during an initial multiplication or later on for rejuvenation after some years of storage, if seed stocks are running low, or there are signs that seed viability may be declining.

At IRRI, in Los Baños south of Manila, we were faced with managing a large germplasm collection of rice lines from all over Asia, from Africa, and South America as well. And these had been collected over a very broad latitudinal range, while Los Baños sits at around 14ºN. We were attempting to grow in a single location many different rice lines, some of which had evolved under more temperate conditions, under different temperature regimes and daylengths.

Kameswara Rao

With my colleague Dr Kameswara Rao (and Professor Richard Ellis from the University of Reading, UK) we spent three years carefully analyzing the effects of different growing environments on seed quality for conservation. Just look for publications here under our names to check out what we achieved. The important changes we made to how we grew rice lines for optimum seed quality have endured until today, although (as I have reported elsewhere) changes to post-harvest handling of seeds have been improved through the work of former IRRI seed physiologist, Dr Fiona Hay.

So, as you can see, there are many different, and interesting, facets to plant sex. And as plant breeders and gene conservationists, we aim to exploit the idiosyncrasies of each species to produce more productive crop varieties or ensure the long term survival of varieties that no longer find favor with farmers, or wild species whose habitats are threatened through agricultural expansion, increasing urbanization, or climate change.