Mutations in a circadian regulator contribute to crop adaptation

Ben Trevaskis CSIRO Plant Industry, Black Mountain ACT 2601, Australia

Plants growing in temperate regions respond to seasonal changes in day length and temperature to coordinate flowering with optimal conditions. Variation in sensitivity or responsiveness to seasonal cues contributes to adaptation to different latitudes and climates by adjusting seasonal flowering behaviour to suit local conditions, allowing some plant species to occupy broad geographical ranges. Variation in seasonal flowering behaviour has also been harnessed in agriculture to produce crop varieties suited to different climates and geographical regions, and also varying sowing dates in the case of annual crops.

A recent study by Weller et al. (2012) examined the molecular basis for different day length requirements in peas (Pisum sativum). The wild ancestral forms of pea typically germinate in autumn and grow vegetatively through winter before flowering in response to increasing day length in spring. Under controlled conditions, accessions with the ancestral flowering behaviour are late flowering in short days. Many modern field pea varieties have a reduced requirement for long days and so flower rapidly in either short or long days. This flowering behaviour allows crops to be grown where the requirement for long days would not be met, at low latitudes for example, or where rapid crop cycling is required irrespective of daylength; such as northern latitudes where crops are sown in spring to avoid harsh winter conditions.

By investigating the molecular basis for variation in day length sensitivity amongst different accessions of pea, Weller et al. (2012) identified two loci that contribute to reduced long-day requirement. One of these loci was mapped to a loss-of-function mutation in the pea orthologue of the Arabidopsis EARLY FLOWERING 3 (ELF3) gene. This is consistent with the functional role of ELF3 in Arabidopsis; loss-of-function mutations in ELF3 cause early flowering in Arabidopsis grown in short days (Zagotta et al., 1996).  Arabidopsis, like pea, is normally late flowering in short days. Haplotype analysis suggests that a loss-of-function mutation in ELF3 that is now broadly distributed in modern varieties arose in a common ancestor, and has been selected in peas grown in regions where crops are grown in short day lengths or where rapid cycling is beneficial. Weller et al. (2012) also showed that a loss-of-function mutation in ELF3 is linked to reduced long day requirement in lentils (Lens culinaris), another temperate legume crop.

The apparent contribution of a loss-of-function mutation in ELF3 to range expansion of pea has a parallel in temperate cereals. Loss-of-function mutations in the barley ELF3 gene cause early flowering in short days, and have been used to adapt barley cultivars to different growing regions (Faure et al., 2012; Zakhrabekova et al.,2012). For example, a ELF3 loss of function mutation generated in a Swedish mutagenesis breeding program was used to breed fast cycling, day length insensitive barleys that can be grown in areas with short spring/summer growing seasons in Nordic countries (Zakhrabekova et al., 2012).

The early flowering phenotype of Arabidopsis elf3 mutants is associated with elevated expression of the FLOWERING LOCUS T (FT) (Suarez-Lopez et al., 2001). FT is a potent promoter of flowering that is normally expressed in long days to trigger the long-day flowering response, so high levels of FT expression can explain the early flowering of elf3 mutants in short days. Although the molecular mechanism underlying the early flowering phenotype of the pea ELF3 loss-of-function mutants is unclear, a similar molecular mechanism seems likely (see Hecht et al., (2011) for more details of the role of FT–like genes in flowering time control in pea). Mutations in the Arabidopsis ELF3 gene also disrupt circadian rhythms (Hicks et al., 1996). Both pea and barley ELF3 mutants exhibit similar disruption of circadian rhythms (Faure et al., 2012, Weller et al., 2012; Zakhrabekova et al., 2012). This raises interesting questions:
How critical is the circadian clock for the cultivation of crops? How many circadian functions can be lost to produce different flowering behaviours before plant performance is compromised? Potentially the cultivation of crops in managed environments has allowed the loss of diurnal rhythms, at least in some growing regions. This will be an interesting area for future research.

The recent finding that the ELF3 gene is a major determinant of reduced long-day requirement in temperate legumes and temperate cereals is a fine example of how knowledge generated in model systems can be applied to increase our understanding of crop biology. This research will have direct impact on crop breeding programmes by facilitating marker assisted selection and by allowing rapid screening for allelic diversity through gene re-sequencing.

References

Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA. 2012. Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. PNAS 109, 8328-8333.

Hecht V, Laurie RE, Vander Schoor JK, Ridge S, Knowles CL, Liew LC, Sussmilch FC, Murfet IC, Macknight RC, Weller JL. 2011. The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23, 147-161.

Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA. 1996. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274, 790-792.

Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116-1120.

Weller JL, Liew LC, Hecht VF, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C, Dalmais M, Rameau C, Bendahmane A, Macknight RC, Lejeune-Hénaut I. 2012. A conserved molecular basis for photoperiod adaptation in two temperate legumes.www.pnas.org/cgi/doi/10.1073/pnas.1207943110.

Zagotta MT, Hicks KA, Jacobs CI, Young JC, Hangarter RP, Meeks-Wagner DR.1996. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant Journal 10, 691-701.

Zakhrabekova S, Gough SP, Braumann I, Müller AH, Lundqvist J, Ahmann K, Dockter C, Matyszczak I, Kurowska M, Druka A, Waugh R, Graner A, Stein N, Steuernagel B, Lundqvist U, Hansson M. 2012. Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. PNAS 109, 4326-4331.

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2 Responses to Mutations in a circadian regulator contribute to crop adaptation

  1. Ben Trevaskis says:

    Hi Thomas,

    I think that Arabidopsis has added to our understanding of why elf3 mutations affect the flowering time – not sure that Neolithic farmers knew that adaptation of seasonal flowering responses would overlap with circadian time keepers. Note the wording – “understanding crop biology”.

    As for application – the history of the barley elf3 mutation in the Nordic mutagenesis breeding is a good example. Other uses are parent selection in crosses, marker assisted selection, sequence based diversity screens, and there will be others. Not sure that a specific technique was advocated?

    Hope that clarifies these ideas.

  2. Thomas Björkman says:

    Weller et al. point out that the hr (elf3 ortholog) mutation in pea was selected in prehistoric times, when knowledge generated by model systems was not yet available. More generally, selection for daylength-insensitve crops has been successful in most crops without using molecular tools such as this. The final claim in this highlight (though not in the original paper) is that the new knowledge will be valuable for future breeding. I would be interested to learn which crops currently lack day neutral varieties and in which hr LOF alleles might be discovered as a result of the new information. In other words, while it is a plausible scenario, is there a specific instance where the proposed technique is actually needed?

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