Field Crops Research

Volume 194, 1 August 2016, Pages 103-111
Field Crops Research

Plantain cultivars (Musa spp. AAB) grown at different altitudes demonstrate cool temperature and photoperiod responses relevant to genetic improvement

https://doi.org/10.1016/j.fcr.2016.02.006Get rights and content

Highlights

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    Juvenile and mid-vegetative phases studied.
  • •
    Cool temperatures shorten the juvenile phase.
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    Suckers begin to grow after juvenile phase is completed.
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    Photoperiod response in mid-vegetative phase differs between cultivars.
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    Responses to environment could be manipulated to produce new cultivars.

Abstract

Knowledge of plant development in plantains is needed to manage seasonal variation in production and better match critical development phases with appropriate seasons. Plantains have juvenile, mid-vegetative and floral phases leading up to flowering (bunch emergence). We examined whether the juvenile phase showed a cool temperature response, whether the mid-vegetative phase was sensitive to photoperiod and how these phases were related to growth of lateral shoots (suckers) up to flowering. We examined published data of an experiment of five plantain cultivars grown at four altitudes, and therefore temperatures (1000 m, 24 °C to 2200 m, 16 °C) within 1° latitude of the equator in the Democratic Republic of Congo. Four of the five cultivars showed a cool temperature response in the juvenile phase. Plants grown in cool temperatures (16 °C) ended the juvenile phase after producing 7 leaves. In warmer climates (24 °C) 15 leaves were produced before the juvenile phase ended. All five cultivars demonstrated a high capacity to respond to photoperiod in the mid-vegetative phase. There were detectable differences in capacity of the cultivars to respond to photoperiod, Ps. ‘Vuhindi’ had the least capacity (Ps = 90) and ‘Musilongo’ and ‘Vuhembe’ the greatest (Ps = 145). Across altitudes, suckers began to appear above ground at just after the end of the juvenile phase and there was a strong positive linear correlation (r2 = 0.97) between the calculated phyllochron (10–27 days) and the proportion of lateral buds that grew into suckers. With a phyllochron of 10 days about 10% of the lateral buds present on the plant produced lateral shoots up to flowering. At 27 days, from 40% to 80% of the lateral buds produced suckers depending on the cultivar. The responses of the juvenile phase to low temperature and the mid-vegetative phase to photoperiod in Musa spp. opens the opportunity to alter plant development and produce cultivars better suited to the climates where they are currently grown and to extend this range.

Introduction

Edible bananas and plantains (Musa spp.) are perennial herbs that reproduce vegetatively. In cultivation their production varies seasonally even though growth continues throughout the year. For example, in irrigated plantations in Central America, flowering can vary from 37 to 65 bunches emerged/ha/week in Guatemala and Honduras (15°N) and from 37 to 45 bunches emerged/ha/week, closer to the equator, in Panama (8°N) (Fortescue et al., 2011). For plants grown at the equator in smallholder management systems in Africa the number of bunches produced may vary more than three-fold from one quarter of the year to another (Birabwa et al., 2010). To understand these responses of bananas and plantains in production systems we need to extend our knowledge of their development, moving towards a functional approach.
Temperature, photoperiod and soil water balance (deficit and excess) are primary factors that drive the development of bananas and plantains from planting to flowering (bunch emergence) (Fortescue et al., 2011). Because temperature is the main driver, the progress of development can be measured by using thermal time (C° days) with an appropriate base temperature (Tb) (Turner and Hunt, 1987, Tixier et al., 2004, Fortescue et al., 2011). Thermal time between two developmental events is assumed to be stable for a cultivar across locations and climates, as it is with wheat (Triticum aestivum) for example (Weir et al., 1984, Hay and Kirby, 1991). If temperature was the only driver of plantain development from planting to flowering, then crops with different planting dates at a single location would have the same cumulative thermal time. However, in the field thermal time varies systematically with planting date of plantains and bananas in the tropics and subtropics (Fortescue et al., 2011). Much of this systematic variation is associated with changes in photoperiod and soil water balance that ‘fine-tune’ the response of development to temperature. The impact of factors such as temperature per se, cool temperature, vernalisation, photoperiod (McMaster et al., 2008) or soil water status, on development can be postulated in a model of development by modifying accumulated thermal time with the appropriate empirical coefficients (scalar range 0.0–1.0) to estimate thermal development units. Then, the variation of thermal development units across environments, treatments or locations is minimised (Fortescue et al., 2011). The empirical coefficients, corresponding to factors such as soil water balance or photoperiod, can then be evaluated against independent sets of data. This approach can detect, for example, whether or not cultivars of Musa spp. have a capacity to respond to photoperiod irrespective of the latitude at which they were grown.
To predict a developmental event such as anthesis in wheat modification of the accumulated thermal time has been used by numerous investigators, for example Weir et al. (1984), McMaster et al. (2008) and Bogard et al. (2014). In the work of McMaster et al. (2008) the responses of development rate to temperature per se, vernalisation and photoperiod were of particular interest. Fortescue et al. (2011) used the approach of modifying thermal time to establish the effects of photoperiod and soil water balance on the rate of development of banana and plantain in the tropics and subtropics. Their work supports the view that banana and plantain have a quantitative (facultative) long-day response to photoperiod and respond developmentally to soil water balance. The coefficients of the response to photoperiod used to calculate the appropriate scalar of different genomic groups (AAA, AAB) of Musa spp. (127 ± 4) were about three times higher than published values for wheat (43 ± 5) (McMaster et al., 2008). The high value of this coefficient for banana has the effect of slowing the accumulation of thermal time and thus calculated development. It extends the time taken for a generation of banana to flower, compared with an annual species. Thus, Musa spp. has a high capacity to respond to photoperiod, compared with wheat, perhaps reflecting the ability to use small changes in day-length in tropical regions to coordinate reproductive events. Small changes in day-length can be sensed by rice (Oryza sativa), for example (Dore, 1959) and it appears this is the case for banana. However, unlike rice, which has a short-day obligate response to photoperiod, banana has a facultative, long-day response (Fortescue et al., 2011).
Fortescue et al. (2011) found that bananas and plantain had a phase of development immediately after planting during which they were not sensitive to photoperiod. They called this the juvenile phase and it represented about 50% of the pre-flowering time for crops grown in the tropics and 33% for crops grown at higher latitudes. This is similar to the juvenile (basic vegetative) phase in rice which is not sensitive to photoperiod (Sasamura, 1960). In winter wheat, the equivalent phase is sensitive to vernalisation (Brooking 1996), and wheat may not respond to photoperiod unless the vernalisation requirement is met (McMaster et al., 2008). The genome of Musa acuminata (D’Hont et al., 2013) contains homologues of the genes responsible for vernalisation and sensitivity to photoperiod in wheat and Arabidopsis thaliana (Turner et al., 2015). Whether these genes affect the early developmental response of the bananas and plantains to cool temperature through a mechanism similar to vernalisation is unknown. Classically, vernalisation is associated with temperatures below those normally experienced in tropical and subtropical zones. Indeed, exposure of banana to vernalising temperatures causes chilling damage (Israeli and Lahav, 2000). However, temperatures below 20 °C can stimulate flowering in plants of temperate, tropical and subtropical origin. For example, temperate woody species (King et al., 1992, King, 1998) and mango (Mangifera indica), lychee (Litchi chinensis) and avocado (Persea americana) (Chaikiattiyos et al., 1994).
Each leaf produced by a shoot of banana is associated with a lateral bud, except for the last 11 leaves that are produced on the aerial stem (Barker and Steward, 1962). If they grow into lateral shoots (suckers) they produce the next crop, making the banana a perennial plant. Altitude has a profound effect on the production of suckers in plantain cultivars (INEAC, 1960, Sikyolo et al., 2013). So few suckers appear above ground before flowering at low altitudes that production cycles are very long and plantations do not survive over time (De Langhe et al., 1983, Swennen and Wilson, 1983, Swennen et al., 1984). At high altitude many more lateral buds develop into suckers than at lower altitudes. In wheat, the production of tillers is associated with increased supply of photosynthates and more tillers are present at heading when plants grow in cooler than in warmer temperatures (Friend, 1965). This is similar to the response of sucker production observed in plantains in cool, high altitude environments.
Sikyolo et al. (2013) grew several cultivars of plantain (Musa spp. AAB) at locations with different altitudes (1000–2200 m) and within 1° latitude of the equator in North Kivu, Democratic Republic of Congo. Their purpose was to determine the adaptability of plantains to high altitudes, especially in relation to yield. The phenological data collected in these experiments provide the opportunity to examine the effect of different temperatures (altitude) on plantain development under relatively constant photoperiod for the plant crop of several plantain cultivars. Our objectives were:
First, to determine whether the cultivars of plantain in the experiments of Sikyolo et al. (2013) had the capacity to respond to photoperiod. Our hypothesis was that a capacity to respond to photoperiod would be demonstrated if, for each cultivar, a photoperiod factor accounted for variation between locations in accumulated thermal time.
Second, to investigate the hypothesis that the juvenile phase in plantains would be responsive to temperature: cool temperatures advancing development.
Third, to examine the relationship between sucker production, crop ontogeny and the phyllochron. An extended phyllochron would be a proxy for increased photosynthate supply to the lateral buds at the base of leaves and from which suckers grow. Our hypothesis was that as the phyllochron increased, so there would be an increase in the number of suckers on the parent plant when it bunched. We also explored the relationship between sucker production and crop ontogeny, measured as calculated cumulative leaf production up to flowering.

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Section snippets

Model of development

The developmental model of banana and plantain from planting to bunch emergence adopted here follows that of Fortescue et al. (2011). From date of planting there is a juvenile phase during which the plant is not sensitive to photoperiod. The juvenile phase is followed by a mid-vegetative phase during which the plant becomes sensitive to photoperiod. Floral initiation then occurs and the plant enters a floral phase that ends with flowering when the inflorescence emerges from the top of the

Leaf number

Sites caused larger differences in total leaf number than cultivars (Table 1). At Butembo, with a mean annual temperature of 18.8 °C, about 21 leaves were produced, averaged across cultivars. The plantains grown at Mavivi, the warmest site (23.6 °C), produced many more leaves, 36 in total. The two False Horn plantains, ‘Musilongo’ and ‘Kotina’, produced about 26 leaves, averaged over the four sites. The three French plantains produced more, about 30 leaves, averaged over the four sites (Table 1).

Photoperiod, leaf number and cool temperature response

The inclusion of a photoperiod factor in the calculation of thermal time reduced the coefficient of variation for thermal development units between sites for all five plantain cultivars. This supported the hypothesis that plantain cultivars show sensitivity to photoperiod in the mid-vegetative phase. The sensitivity to photoperiod reduced accumulated thermal development units by 50–75% during the mid-vegetative phase. The response was similar to that observed previously by Fortescue et al.

Acknowledgements

We thank I. Sikyolo, C. Sivirihauma, V. Ndungo and E. De Langhe for access to their data and David Midmore for suggesting the juvenile phase of development in bananas should be investigated. We appreciate comments made by David Midmore, Rony Swennen, Tim Setter and Jane Gibbs on this paper. Joseph Adheka kindly advised us on the classification of the plantain cultivars. Thanks to reviewers who provided helpful and thoughtful comments. This work was linked (GB and WO) to the CGIAR research

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