Azuki translocation under domestication

Azuki bean is an Asian crop with a wide cultivation area (from Japan to the continental China and further West up to Bhutan and Nepal). It has a distinctive red colour and is known in western societies under its characteristic economic preparation: a dense but very sweet paste, among and with many possible culinar uses.

…Apparently, it has been domesticated in Japan about 4000 years ago (this is the oldest archeological evidence of Azuki beans culinary use), and like many crop species, it belongs to a complex where a wild ancestral subspecies (Vigna angularis nipponensis) often coexist with the domesticated form (V. angularis angularis). Strikingly, where the Azuki bean culture is most intensive in Japan (Hokkaido), the wild plant is not found. But it is sometimes frequent in other Japanese regions, where landraces are often grown on a small scale for self consumption. The opportunity for hybridization between the forms is of course reduced because of the natural tendency of Vigna, like many other legumes, to self-fertilize. The outcross rate has nevertheless been shown to be as high as 1% in sympatry, and there are many known occurrence of plants of hybrid descent (sometimes persisting in the wild as complex populations).

The study* from which this post is based has undertaken a dissection of the genetic effects of Azuki bean domestication (in the scientific jargon, this is called a “QTL study”, where the acronym stands for Quantitative Trait Loci, that is genes involved in complex traits). And there are very interesting things that occurred during domestication of this original crop:

-   first, as the title suggests, the domestication syndrome of the plant (its set of special characteristics due to evolution under human selection) is protected by a rearrangement of chromosomes, more precisely a fusion (or more dynamically named, a chromosome translocation) between chromosomes otherwise independent in the undomesticated form. This kind of dramatic reorganization of the genome reduces the opportunities for gene-flow between individuals sharing different organizations. Most genes involved in the phenotypic changes that occurred during domestication are not only clustered (a situation frequently encountered in domestication processes in plants), but also located near the translocation breakpoint. This results in a fairly cohesive phenotypic integration, and offers a protective barrier against introgression from the wild species. As a consequence nevertheless, it is now harder for breeders to possibly integrate potential genes of interest from the wild into the cultivated gene pool. But plant breeding is a difficult art anyway…

 -   Azuki domestication involved a reduction of seed number to increase seed size (this is a rather common trade-off in the plant world; it’s either many small seeds or fewer but bigger ones). Amazingly, domestication had some unexpected effects. Cultivated plants also have bigger leaves, probably because this characteristic was preferred by early Azuki bean farmers. And an increase in leaf size is also negatively correlated with seed numbers in this species. So a reduced seed production was also not only resulting from selection for bigger beans, but maybe from an indirect selection for bigger leaves. This can be understood as a trade-off for resource distribution among organs, and what’s invested in leaves and other seeds is lost for other beans. What’s curious is that, intuitively, we would expect an increased leaf size to yield more photosyntates and thus allow for higher seeds production. But that’s not the case in this specific situation. An example of a domestication paradox?

- last, there’s something striking about seed colour. Given the importance of (cultural) food preferences, we would anticipate the reddish colour of these beans to have been retained by farmers as a matter of taste. Indeed, the very specific colour of Azuki beans is conveniently adding up to its flavour (admittedly, red is attractive). At least, that’s what I would have gladly been thinking.
The thing is, it may have something to do with seeds dormancy instead. Wild Azuki have small black seeds. These have an undeniable quality as wild seeds: they may enter dormancy, which allows over wintering safely. On the other hand, germination is made hazardous. While this is completely benign in nature, this is really not what farmers are interested in. They understandably prefer more homogenous crops where plants germinate, grow, flower and mature fruits at around the same time. Since seeds are over wintering at the farmer’s discretion, a reduced dormancy was selected for to increase field homogeneity. And apparently, as is already described in several other crop species, the seed coat pigments are involved in being more or less water-proof and thus more or less dormant. In conclusion, you can sometimes have it both ways!

Why would all that matter? Well, because Azuki beans are really good!

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* A. Kaga, T. Isemura, N. Tomooka and D. A. Vaughan (2008). The Genetics of Domestication of the Azuki Bean (Vigna angularis). Genetics 178: 1013-1036.

(Image from Wikipedia).