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  1. Masuda S, Tani N, Ueno S, Lee SL, Muhammad N, Kondo T, et al.
    PLoS One, 2013;8(12):e82039.
    PMID: 24391712 DOI: 10.1371/journal.pone.0082039
    Pollinator syndrome is one of the most important determinants regulating pollen dispersal in tropical tree species. It has been widely accepted that the reproduction of tropical forest species, especially dipterocarps that rely on insects with weak flight for their pollination, is positively density-dependent. However differences in pollinator syndrome should affect pollen dispersal patterns and, consequently, influence genetic diversity via the mating process. We examined the pollen dispersal pattern and mating system of Shorea maxwelliana, the flowers of which are larger than those of Shorea species belonging to section Mutica which are thought to be pollinated by thrips (weak flyers). A Bayesian mating model based on the paternity of seeds collected from mother trees during sporadic and mass flowering events revealed that the estimated pollen dispersal kernel and average pollen dispersal distance were similar for both flowering events. This evidence suggests that the putative pollinators - small beetles and weevils - effectively contribute to pollen dispersal and help to maintain a high outcrossing rate even during sporadic flowering events. However, the reduction in pollen donors during a sporadic event results in a reduction in effective pollen donors, which should lead to lower genetic diversity in the next generation derived from seeds produced during such an event. Although sporadic flowering has been considered less effective for outcrossing in Shorea species that depend on thrips for their pollination, effective pollen dispersal by the small beetles and weevils ensures outcrossing during periods of low flowering tree density, as occurs in a sporadic flowering event.
  2. Kobayashi MJ, Ng KKS, Lee SL, Muhammad N, Tani N
    Am J Bot, 2020 11;107(11):1491-1503.
    PMID: 33190268 DOI: 10.1002/ajb2.1557
    PREMISE: Leaf phenology is an essential developmental process in trees and an important component in understanding climate change. However, little is known about the regulation of leaf phenology in tropical trees.

    METHODS: To understand the regulation by temperature of leaf phenology in tropical trees, we performed daily observations of leaf production under rainfall-independent conditions using saplings of Shorea leprosula and Neobalanocarpus heimii, both species of Dipterocarpaceae, a dominant tree family of Southeast Asia. We analyzed the time-series data obtained using empirical dynamic modeling (EDM) and conducted growth chamber experiments.

    RESULTS: Leaf production by dipterocarps fluctuated in the absence of fluctuation in rainfall, and the peaks of leaf production were more frequent than those of day length, suggesting that leaf production cannot be fully explained by these environmental factors, although they have been proposed as regulators of leaf phenology in dipterocarps. Instead, EDM suggested a causal relationship between temperature and leaf production in dipterocarps. Leaf production by N. heimii saplings in chambers significantly increased when temperature was increased after long-term low-temperature treatment. This increase in leaf production was observed even when only nighttime temperature was elevated, suggesting that the effect of temperature on development is not mediated by photosynthesis.

    CONCLUSIONS: Because seasonal variation in temperature in the tropics is small, effects on leaf phenology have been overlooked. However, our results suggest that temperature is a regulator of leaf phenology in dipterocarps. This information will contribute to better understanding of the effects of climate change in the tropics.

  3. Tani N, Tsumura Y, Kado T, Taguchi Y, Lee SL, Muhammad N, et al.
    Ann Bot, 2009 Dec;104(7):1421-34.
    PMID: 19808773 DOI: 10.1093/aob/mcp252
    BACKGROUND AND AIMS: Knowledge of pollen dispersal patterns and variation of fecundity is essential to understanding plant evolutionary processes and to formulating strategies to conserve forest genetic resources. Nevertheless, the pollen dispersal pattern of dipterocarp, main canopy tree species in palaeo-tropical forest remains unclear, and flowering intensity variation in the field suggests heterogeneity of fecundity.

    METHODS: Pollen dispersal patterns and male fecundity variation of Shorea leprosula and Shorea parvifolia ssp. parvifolia on Peninsular Malaysian were investigated during two general flowering seasons (2001 and 2002), using a neighbourhood model modified by including terms accounting for variation in male fecundity among individual trees to express heterogeneity in flowering.

    KEY RESULTS: The pollen dispersal patterns of the two dipterocarp species were affected by differences in conspecific tree flowering density, and reductions in conspecific tree flowering density led to an increased selfing rate. Active pollen dispersal and a larger number of effective paternal parents were observed for both species in the season of greater magnitude of general flowering (2002).

    CONCLUSIONS: The magnitude of general flowering, male fecundity variation, and distance between pollen donors and mother trees should be taken into account when attempting to predict the effects of management practices on the self-fertilization and genetic structure of key tree species in tropical forest, and also the sustainability of possible management strategies, especially selective logging regimes.

  4. Tani N, Abdul Hamid ZA, Joseph N, Sulaiman O, Hashim R, Arai T, et al.
    Sci Rep, 2020 01 20;10(1):650.
    PMID: 31959766 DOI: 10.1038/s41598-019-57170-8
    Oil palm is an important crop for global vegetable oil production, and is widely grown in the humid tropical regions of Southeast Asia. Projected future climate change may well threaten palm oil production. However, oil palm plantations currently produce large amounts of unutilised biological waste. Oil palm stems - which comprise two-thirds of the waste - are especially relevant because they can contain high levels of non-structural carbohydrates (NSC) that can serve as feedstock for biorefineries. The NSC in stem are also considered a potent buffer to source-sink imbalances. In the present study, we monitored stem NSC levels and female reproductive growth. We then applied convergent cross mapping (CCM) to assess the causal relationship between the time-series. Mutual causal relationships between female reproductive growth and the stem NSC were detected, with the exception of a relationship between female reproductive organ growth and starch levels. The NSC levels were also influenced by long-term cumulative temperature, with the relationship showing a seven-month time lag. The dynamic between NSC levels and long-term cumulative rainfall showed a shorter time lag. The lower temperatures and higher cumulative rainfall observed from October to December identify this as a period with maximum stem NSC stocks.
  5. Yeoh SH, Satake A, Numata S, Ichie T, Lee SL, Basherudin N, et al.
    Mol Ecol, 2017 Oct;26(19):5074-5085.
    PMID: 28749031 DOI: 10.1111/mec.14257
    Elucidating the physiological mechanisms of the irregular yet concerted flowering rhythm of mass flowering tree species in the tropics requires long-term monitoring of flowering phenology, exogenous and endogenous environmental factors, as well as identifying interactions and dependencies among these factors. To investigate the proximate factors for floral initiation of mast seeding trees in the tropics, we monitored the expression dynamics of two key flowering genes, meteorological conditions and endogenous resources over two flowering events of Shorea curtisii and Shorea leprosula in the Malay Peninsula. Comparisons of expression dynamics of genes studied indicated functional conservation of FLOWERING LOCUS T (FT) and LEAFY (LFY) in Shorea. The genes were highly expressed at least 1 month before anthesis for both species. A mathematical model considering the synergistic effect of cool temperature and drought on activation of the flowering gene was successful in predicting the observed gene expression patterns. Requirement of both cool temperature and drought for floral transition suggested by the model implies that flowering phenologies of these species are sensitive to climate change. Our molecular phenology approach in the tropics sheds light on the conserved role of flowering genes in plants inhabiting different climate zones and can be widely applied to dissect the flowering processes in other plant species.
  6. Kondo T, Nishimura S, Tani N, Ng KK, Lee SL, Muhammad N, et al.
    Am J Bot, 2016 Nov;103(11):1912-1920.
    PMID: 27797714
    PREMISE OF THE STUDY: In tropical rainforests of Southeast Asia, a highly fecund thrips (Thrips spp.) responds rapidly to the mass flowering at multiple-year intervals characteristic of certain species such as the canopy tree studied here, Shorea acuminata, by feeding on flower resources. However, past DNA analyses of pollen adherent to thrips bodies revealed that the thrips promoted a very high level of self-pollination. Here, we identified the pollinator that contributes to cross-pollination and discuss ways that the pollination system has adapted to mass flowering.

    METHODS: By comparing the patterns of floral visitation and levels of genetic diversity in adherent pollen loads among floral visitors, we evaluated the contribution of each flower visitor to pollination.

    KEY RESULTS: The big-eyed bug, Geocoris sp., a major thrips predator, was an inadvertent pollinator, and importantly contributed to cross-pollination. The total outcross pollen adhering to thrips was approximately 30% that on the big-eyed bugs. Similarly, 63% of alleles examined in S. acuminata seeds and seedlings occurred in pollen adhering to big-eyed bugs; about 30% was shared with pollen from thrips.

    CONCLUSIONS: During mass flowering, big-eyed bugs likely travel among flowering S. acuminata trees, attracted by the abundant thrips. Floral visitation patterns of big-eyed bugs vs. other insects suggest that these bugs can maintain their population size between flowering by preying upon another thrips (Haplothrips sp.) that inhabits stipules of S. acuminata throughout the year and quickly respond to mass flowering. Thus, thrips and big-eyed bugs are essential components in the pollination of S. acuminata.

  7. Ohtani M, Kondo T, Tani N, Ueno S, Lee LS, Ng KK, et al.
    Mol Ecol, 2013 Apr;22(8):2264-79.
    PMID: 23432376 DOI: 10.1111/mec.12243
    Tropical rainforests in South-East Asia have been affected by climatic fluctuations during past glacial eras. To examine how the accompanying changes in land areas and temperature have affected the genetic properties of rainforest trees in the region, we investigated the phylogeographic patterns of a widespread dipterocarp species, Shorea leprosula. Two types of DNA markers were used: expressed sequence tag-based simple sequence repeats and chloroplast DNA (cpDNA) sequence variations. Both sets of markers revealed clear genetic differentiation between populations in Borneo and those in the Malay Peninsula and Sumatra (Malay/Sumatra). However, in the south-western part of Borneo, genetic admixture of the lineages was observed in the two marker types. Coalescent simulation based on cpDNA sequence variation suggested that the two lineages arose 0.28-0.09 million years before present and that following their divergence migration from Malay/Sumatra to Borneo strongly exceeded migration in the opposite direction. We conclude that the genetic structure of S. leprosula was largely formed during the middle Pleistocene and was subsequently modified by eastward migration across the subaerially exposed Sunda Shelf.
  8. Ng KKS, Lee SL, Tnah LH, Nurul-Farhanah Z, Ng CH, Lee CT, et al.
    Forensic Sci Int Genet, 2016 07;23:197-209.
    PMID: 27213560 DOI: 10.1016/j.fsigen.2016.05.002
    Illegal logging and smuggling of Gonystylus bancanus (Thymelaeaceae) poses a serious threat to this fragile valuable peat swamp timber species. Using G. bancanus as a case study, DNA markers were used to develop identification databases at the species, population and individual level. The species level database for Gonystylus comprised of an rDNA (ITS2) and two cpDNA (trnH-psbA and trnL) markers based on a 20 Gonystylus species database. When concatenated, taxonomic species recognition was achieved with a resolution of 90% (18 out of the 20 species). In addition, based on 17 natural populations of G. bancanus throughout West (Peninsular Malaysia) and East (Sabah and Sarawak) Malaysia, population and individual identification databases were developed using cpDNA and STR markers respectively. A haplotype distribution map for Malaysia was generated using six cpDNA markers, resulting in 12 unique multilocus haplotypes, from 24 informative intraspecific variable sites. These unique haplotypes suggest a clear genetic structuring of West and East regions. A simulation procedure based on the composition of the samples was used to test whether a suspected sample conformed to a given regional origin. Overall, the observed type I and II errors of the databases showed good concordance with the predicted 5% threshold which indicates that the databases were useful in revealing provenance and establishing conformity of samples from West and East Malaysia. Sixteen STRs were used to develop the DNA profiling databases for individual identification. Bayesian clustering analyses divided the 17 populations into two main genetic clusters, corresponding to the regions of West and East Malaysia. Population substructuring (K=2) was observed within each region. After removal of bias resulting from sampling effects and population subdivision, conservativeness tests showed that the West and East Malaysia databases were conservative. This suggests that both databases can be used independently for random match probability estimation within respective regions. The reliability of the databases was further determined by independent self-assignment tests based on the likelihood of each individual's multilocus genotype occurring in each identified population, genetic cluster and region with an average percentage of correctly assigned individuals of 54.80%, 99.60% and 100% respectively. Thus, after appropriate validation, the genetic identification databases developed for G. bancanus in this study could support forensic applications and help safeguard this valuable species into the future.
  9. Tani N, Tsumura Y, Fukasawa K, Kado T, Taguchi Y, Lee SL, et al.
    PLoS One, 2015;10(5):e0123445.
    PMID: 25938512 DOI: 10.1371/journal.pone.0123445
    The maintenance of mixed mating was studied in Shorea curtisii, a dominant and widely distributed dipterocarp species in Southeast Asia. Paternity and hierarchical Bayesian analyses were used to estimate the parameters of pollen dispersal kernel, male fecundity and self-pollen affinity. We hypothesized that partial self incompatibility and/or inbreeding depression reduce the number of selfed seeds if the mother trees receive sufficient pollen, whereas reproductive assurance increases the numbers of selfed seeds under low amounts of pollen. Comparison of estimated parameters of self-pollen affinity between high density undisturbed and low density selectively logged forests indicated that self-pollen was selectively excluded from mating in the former, probably due to partial self incompatibility or inbreeding depression until seed maturation. By estimating the self-pollen affinity of each mother tree in both forests, mother trees with higher amount of self-pollen indicated significance of self-pollen affinity with negative estimated value. The exclusion of self-fertilization and/or inbreeding depression during seed maturation occurred in the mother trees with large female fecundity, whereas reproductive assurance increased self-fertilization in the mother trees with lower female fecundity.
  10. Suhaimi AH, Kobayashi MJ, Satake A, Ng CC, Lee SL, Muhammad N, et al.
    PeerJ, 2023;11:e16368.
    PMID: 38047035 DOI: 10.7717/peerj.16368
    Climatic factors have commonly been attributed as the trigger of general flowering, a unique community-level mass flowering phenomenon involving most dipterocarp species that forms the foundation of Southeast Asian tropical rainforests. This intriguing flowering event is often succeeded by mast fruiting, which provides a temporary yet substantial burst of food resources for animals, particularly frugivores. However, the physiological mechanism that triggers general flowering, particularly in dipterocarp species, is not well understood largely due to its irregular and unpredictable occurrences in the tall and dense forests. To shed light on this mechanism, we employed ecological transcriptomic analyses on an RNA-seq dataset of a general flowering species, Shorea curtisii (Dipterocarpaceae), sequenced from leaves and buds collected at multiple vegetative and flowering phenological stages. We assembled 64,219 unigenes from the transcriptome of which 1,730 and 3,559 were differentially expressed in the leaf and the bud, respectively. Differentially expressed unigene clusters were found to be enriched with homologs of Arabidopsis thaliana genes associated with response to biotic and abiotic stresses, nutrient level, and hormonal treatments. When combined with rainfall data, our transcriptome data reveals that the trees were responding to a brief period of drought prior to the elevated expression of key floral promoters and followed by differential expression of unigenes that indicates physiological changes associated with the transition from vegetative to reproductive stages. Our study is timely for a representative general flowering dipterocarp species that occurs in forests that are under the constant threat of deforestation and climate change as it pinpoints important climate sensitive and flowering-related homologs and offers a glimpse into the cascade of gene expression before and after the onset of floral initiation.
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