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1.  ContentSnapshots 
Annals of Botany  2013;112(1):i-iii.
doi:10.1093/aob/mct136
PMCID: PMC3691000
2.  Plant Cuttings 
Annals of Botany  2013;112(1):iv-vi.
doi:10.1093/aob/mct137
PMCID: PMC3691001
3.  An invasive Mimosa in India does not adopt the symbionts of its native relatives 
Annals of Botany  2013;112(1):179-196.
Background and Aims
The large monophyletic genus Mimosa comprises approx. 500 species, most of which are native to the New World, with Central Brazil being the main centre of radiation. All Brazilian Mimosa spp. so far examined are nodulated by rhizobia in the betaproteobacterial genus Burkholderia. Approximately 10 Mya, transoceanic dispersal resulted in the Indian subcontinent hosting up to six endemic Mimosa spp. The nodulation ability and rhizobial symbionts of two of these, M. hamata and M. himalayana, both from north-west India, are here examined, and compared with those of M. pudica, an invasive species.
Methods
Nodules were collected from several locations, and examined by light and electron microscopy. Rhizobia isolated from them were characterized in terms of their abilities to nodulate the three Mimosa hosts. The molecular phylogenetic relationships of the rhizobia were determined by analysis of 16S rRNA, nifH and nodA gene sequences.
Key Results
Both native Indian Mimosa spp. nodulated effectively in their respective rhizosphere soils. Based on 16S rRNA, nifH and nodA sequences, their symbionts were identified as belonging to the alphaproteobacterial genus Ensifer, and were closest to the ‘Old World’ Ensifer saheli, E. kostiensis and E. arboris. In contrast, the invasive M. pudica was predominantly nodulated by Betaproteobacteria in the genera Cupriavidus and Burkholderia. All rhizobial strains tested effectively nodulated their original hosts, but the symbionts of the native species could not nodulate M. pudica.
Conclusions
The native Mimosa spp. in India are not nodulated by the Burkholderia symbionts of their South American relatives, but by a unique group of alpha-rhizobial microsymbionts that are closely related to the ‘local’ Old World Ensifer symbionts of other mimosoid legumes in north-west India. They appear not to share symbionts with the invasive M. pudica, symbionts of which are mostly beta-rhizobial.
doi:10.1093/aob/mct112
PMCID: PMC3690997  PMID: 23712450
Mimosa hamata; Mimosa himalayana; Mimosa pudica; Thar Desert; nodulation; Cupriavidus; Burkholderia; Ensifer; bacterial symbionts; rhizobia; Betaproteobacteria; nitrogen fixation; arid regions
4.  Photosynthesis research protocols 
Annals of Botany  2013;112(1):vi-vii.
doi:10.1093/aob/mct113
PMCID: PMC3690998
5.  The evolution of plant form 
Annals of Botany  2013;112(1):vii-viii.
doi:10.1093/aob/mct116
PMCID: PMC3690999
6.  Variation of microsporogenesis in monocots producing monosulcate pollen grains 
Annals of Botany  2013;112(1):135-139.
Background and Aims
Microsporogenesis leading to monosulcate pollen grains has already been described for a wide range of monocot species. However, a detailed study of additional callose deposition after the completion of the cleavage walls has been neglected so far. The study of additional callose deposition in monosulcate pollen grain has gained importance since a correlation between additional callose deposition and aperture location has recently been revealed.
Methods
Microsporogenesis is described for 30 species belonging to eight families of the monocots: Acoraceae, Amaryllidaceae, Alstroemeriaceae, Asparagaceae, Butomaceae, Commelinaceae, Liliaceae and Xanthorrhoeaceae.
Key Results
Five different microsporogenesis pathways are associated with monosulcate pollen grain. They differ in the type of cytokinesis, tetrad shape, and the presence and shape of additional callose deposition. Four of them present additional callose deposition.
Conclusions
In all these different microsporogenesis pathways, aperture location seems to be linked to the last point of callose deposition.
doi:10.1093/aob/mct104
PMCID: PMC3690993  PMID: 23666889
Callose; microsporogenesis; pollen; aperture pattern; monocots; Acoraceae; Amaryllidaceae; Alstroemeriaceae; Asparagaceae; Butomaceae; Commelinaceae; Liliaceae; Xanthorrhoeaceae
7.  Comparative molecular cytogenetic analyses of a major tandemly repeated DNA family and retrotransposon sequences in cultivated jute Corchorus species (Malvaceae) 
Annals of Botany  2013;112(1):123-134.
Background and Aims
The cultivated jute species Corchorus olitorius and Corchorus capsularis are important fibre crops. The analysis of repetitive DNA sequences, comprising a major part of plant genomes, has not been carried out in jute but is useful to investigate the long-range organization of chromosomes. The aim of this study was the identification of repetitive DNA sequences to facilitate comparative molecular and cytogenetic studies of two jute cultivars and to develop a fluorescent in situ hybridization (FISH) karyotype for chromosome identification.
Methods
A plasmid library was generated from C. olitorius and C. capsularis with genomic restriction fragments of 100–500 bp, which was complemented by targeted cloning of satellite DNA by PCR. The diversity of the repetitive DNA families was analysed comparatively. The genomic abundance and chromosomal localization of different repeat classes were investigated by Southern analysis and FISH, respectively. The cytosine methylation of satellite arrays was studied by immunolabelling.
Key Results
Major satellite repeats and retrotransposons have been identified from C. olitorius and C. capsularis. The satellite family CoSat I forms two undermethylated species-specific subfamilies, while the long terminal repeat (LTR) retrotransposons CoRetro I and CoRetro II show similarity to the Metaviridea of plant retroelements. FISH karyotypes were developed by multicolour FISH using these repetitive DNA sequences in combination with 5S and 18S–5·8S–25S rRNA genes which enable the unequivocal chromosome discrimination in both jute species.
Conclusions
The analysis of the structure and diversity of the repeated DNA is crucial for genome sequence annotation. The reference karyotypes will be useful for breeding of jute and provide the basis for karyotyping homeologous chromosomes of wild jute species to reveal the genetic and evolutionary relationship between cultivated and wild Corchorus species.
doi:10.1093/aob/mct103
PMCID: PMC3690992  PMID: 23666888
Corchorus olitorius; Corchorus capsularis; jute; karyotype; satellite DNA; FISH; physical mapping; DNA methylation; immunolabelling
8.  Are there pollination syndromes in the Australian epacrids (Ericaceae: Styphelioideae)? A novel statistical method to identify key floral traits per syndrome 
Annals of Botany  2013;112(1):141-149.
Background and Aims
Convergent floral traits hypothesized as attracting particular pollinators are known as pollination syndromes. Floral diversity suggests that the Australian epacrid flora may be adapted to pollinator type. Currently there are empirical data on the pollination systems for 87 species (approx. 15 % of Australian epacrids). This provides an opportunity to test for pollination syndromes and their important morphological traits in an iconic element of the Australian flora.
Methods
Data on epacrid–pollinator relationships were obtained from published literature and field observation. A multivariate approach was used to test whether epacrid floral attributes related to pollinator profiles. Statistical classification was then used to rank floral attributes according to their predictive value. Data sets excluding mixed pollination systems were used to test the predictive power of statistical classification to identify pollination models.
Key Results
Floral attributes are correlated with bird, fly and bee pollination. Using floral attributes identified as correlating with pollinator type, bird pollination is classified with 86 % accuracy, red flowers being the most important predictor. Fly and bee pollination are classified with 78 and 69 % accuracy, but have a lack of individually important floral predictors. Excluding mixed pollination systems improved the accuracy of the prediction of both bee and fly pollination systems.
Conclusions
Although most epacrids have generalized pollination systems, a correlation between bird pollination and red, long-tubed epacrids is found. Statistical classification highlights the relative importance of each floral attribute in relation to pollinator type and proves useful in classifying epacrids to bird, fly and bee pollination systems.
doi:10.1093/aob/mct105
PMCID: PMC3690994  PMID: 23681546
Epacridaceae (epacrids); Ericaceae; multivariate analysis; plant–pollinator interactions; pollination syndromes; Random Forests; statistical classification; Styphelioideae
9.  The abrupt climate change at the Eocene–Oligocene boundary and the emergence of South-East Asia triggered the spread of sapindaceous lineages 
Annals of Botany  2013;112(1):151-160.
Background and Aims
Paleoclimatic data indicate that an abrupt climate change occurred at the Eocene–Oligocene (E–O) boundary affecting the distribution of tropical forests on Earth. The same period has seen the emergence of South-East (SE) Asia, caused by the collision of the Eurasian and Australian plates. How the combination of these climatic and geomorphological factors affected the spatio-temporal history of angiosperms is little known. This topic is investigated by using the worldwide sapindaceous clade as a case study.
Methods
Analyses of divergence time inference, diversification and biogeography (constrained by paleogeography) are applied to a combined plastid and nuclear DNA sequence data set. Biogeographical and diversification analyses are performed over a set of trees to take phylogenetic and dating uncertainty into account. Results are analysed in the context of past climatic fluctuations.
Key Results
An increase in the number of dispersal events at the E–O boundary is recorded, which intensified during the Miocene. This pattern is associated with a higher rate in the emergence of new genera. These results are discussed in light of the geomorphological importance of SE Asia, which acted as a tropical bridge allowing multiple contacts between areas and additional speciation across landmasses derived from Laurasia and Gondwana.
Conclusions
This study demonstrates the importance of the combined effect of geomorphological (the emergence of most islands in SE Asia approx. 30 million years ago) and climatic (the dramatic E–O climate change that shifted the tropical belt and reduced sea levels) factors in shaping species distribution within the sapindaceous clade.
doi:10.1093/aob/mct106
PMCID: PMC3690995  PMID: 23723259
Biogeography; climate change; diversification; Eocene–Oligocene boundary; Sapindaceae; South-East Asia
10.  Floral ontogeny and gene protein localization rules out euanthial interpretation of reproductive units in Lepironia (Cyperaceae, Mapanioideae, Chrysitricheae) 
Annals of Botany  2013;112(1):161-177.
Background and Aims
In the sedge subfamily Mapanioideae there are considerable discrepancies between the standard trimerous monocot floral architecture expected and the complex floral and inflorescence morphologies seen. Decades of debate about whether the basic reproductive units are single flowers or pseudanthia have not resolved the question. This paper evaluates current knowledge about Mapaniid reproductive structures and presents an ontogenetic study of the Mapaniid genus Lepironia with the first floral protein expression maps for the family, localizing the products of the APETALA1/FRUITFULL-like (AP1/FUL) MADS-box genes with the aim of shedding light on this conundrum.
Methods
A range of reproductive developmental stages, from spikelet primordia through to infructescence material, were processed for anatomical and immunohistochemical analyses.
Key Results
The basic reproductive unit is subtended by a bract and possesses two prophyll-like structures, the first organs to be initiated on the primordium, which grow rapidly, enclosing two whorls of initiating leaf-like structures with intervening stamens and a central gynoecium, formed from an annular primordium. The subtending bract and prophyll-like structures possess very different morphologies from that of the internal leaf-like structures and do not show AP1/FUL-like protein localization, which is otherwise strongly localized in the internal leaf-like structures, stamens and gynoecia.
Conclusions
Results support the synanthial hypothesis as the evolutionary origin of the reproductive unit. Thus, the basic reproductive unit in Lepironia is an extremely condensed pseudanthium, of staminate flowers surrounding a central terminal pistillate female flower. Early in development the reproductive unit becomes enclosed by a split-prophyll, with the whole structure subtended by a bract.
doi:10.1093/aob/mct111
PMCID: PMC3690996  PMID: 23723258
Floral development; Lepironia articulata; Mapanioideae; Chrysitricheae; Cyperaceae; Hypolytreae; SEM; immunolocalization; AP1-FUL-like MADS-box genes
11.  Hydraulic resistance of developing Actinidia fruit 
Annals of Botany  2013;112(1):197-205.
Background and Aims
Xylem flows into most fruits decline as the fruit develop, with important effects on mineral and carbohydrate accumulation. It has been hypothesized that an increase in xylem hydraulic resistance (RT) contributes to this process. This study examined changes in RT that occur during development of the berry of kiwifruit (Actinidia deliciosa), identified the region within the fruit where changes were occurring, and tested whether a decrease in irradiance during fruit development caused an increase in RT, potentially contributing to decreased mineral accumulation in shaded fruit.
Methods
RT was measured using pressure chamber and flow meter methods, the two methods were compared, and the flow meter was also used to partition RT between the pedicel, receptacle and proximal and distal portions of the berry. Dye was used as a tracer for xylem function. Artificial shading was used to test the effect of light on RT, dye entry and mineral accumulation.
Key Results
RT decreased during the early phase of rapid fruit growth, but increased again as the fruit transitioned to a final period of slower growth. The most significant changes in resistance occurred in the receptacle, which initially contributed 20 % to RT, increasing to 90 % later in development. Dye also ceased moving beyond the receptacle from 70 d after anthesis. The two methods for measuring RT agreed in terms of the direction and timing of developmental changes in RT, but pressure chamber measurements were consistently higher than flow meter estimates of RT, prompting questions regarding which method is most appropriate for measuring fruit RT. Shading had no effect on berry growth but increased RT and decreased dye movement and calcium concentration.
Conclusions
Increased RT in the receptacle zone coincides with slowing fresh weight growth, reduced transpiration and rapid starch accumulation by the fruit. Developmental changes in RT may be connected to changes in phloem functioning and the maintenance of water potential gradients between the stem and the fruit. The effect of shade on RT extends earlier reports that shading can affect fruit vascular differentiation, xylem flows and mineral accumulation independently of effects on transpiration.
doi:10.1093/aob/mct101
PMCID: PMC3690990  PMID: 23658370
Calcium concentration; dye tracer; hydraulic resistance; partitioning of fruit resistance; shade; Actinidia deliciosa; kiwifruit
12.  Time-lapse imaging of self- and cross-pollinations in Brassica rapa 
Annals of Botany  2013;112(1):115-122.
Background and Aims
Pollination is an important process in the life cycle of plants and is the first step in bringing together the male and female gametophytes for plant reproduction. While pollination has been studied for many years, accurate knowledge of the morphological aspects of this process is still far from complete. This study therefore focuses on a morphological characterization of pollination, using time-series image analysis of self- and cross-pollinations in Brassica rapa.
Methods
Time-lapse imaging of pollen behaviour during self- and cross-pollinations was recorded for 90 min, at 1 min intervals, using a stereoscopic microscope. Using time-series digital images of pollination, characteristic features of pollen behaviours during self- and cross-pollinations were studied.
Key Results
Pollen exhibited various behaviours in both self- and cross-pollinations, and these were classified into six representative patterns: germination, expansion, contraction, sudden contraction, pulsation and no change. It is noteworthy that in ‘contraction’ pollen grains shrunk within a short period of 30–50 min, and in ‘pulsation’ repeated expansion and contraction occurred with an interval of 10 min, suggesting that a dehydration system is operating in pollination. All of the six patterns were observed on an individual stigma with both self- and cross-pollinations, and the difference between self- and cross-pollinations was in the ratios of the different behaviours. With regard to water transport to and from pollen grains, this occurred in multiple steps, before, during and after hydration. Thus, pollination is regulated by a combination of multiple components of hydration, rehydration and dehydration systems.
Conclusions
Regulated hydration of pollen is a key process for both pollination and self-incompatibility, and this is achieved by a balanced complex of hydration, dehydration and nutrient supply to pollen grains from stigmatic papilla cells.
doi:10.1093/aob/mct102
PMCID: PMC3690991  PMID: 23644359
Brassicaceae; Brassica rapa; pollination; live imaging; pollen hydration; pollen–stigma interaction; self-incompatibility; time-lapse imaging
13.  Peduncles elicit large-mammal endozoochory in a dry-fruited plant 
Annals of Botany  2013;112(1):85-93.
Background and Aims
Plants have evolved a variety of seed dispersal mechanisms to overcome lack of mobility. Many species embed seeds in fleshy pulp to elicit endozoochory, i.e. disseminating seed through the animal gut. In contrast to well-studied fleshy fruited plants, dry-fruited plants may exploit this dispersal mutualism by producing fleshy appendages as a nutritional reward to entice animals to swallow their diaspores, but this has been little studied. In this study, it is hypothesized that these accessory fruits represent co-adaptations facilitating the syndrome of mammalian endozoochorous dispersal.
Methods
Field observations (focal tree watches, faecal surveys and fruiting phenology) with experimental manipulations (examination of seed germination and feeding trials) were conducted over 2 years in a native population of the raisin tree, Hovenia dulcis, which produces enlarged, twisted brown peduncles with external black seeds, in central China.
Key Results
Birds were not observed to swallow seeds or carry infructescences away during 190 h of focal tree watches. However, H. dulcis seeds were detected in 247 faecal samples, representative of two herbivore and four carnivore mammalian species. Feeding trials revealed that peduncles attracted mammals to consume the entire infructescence, thereby facilitating effective seed dispersal. The germination rate of egested seeds proved higher than that of unconsumed seeds. It was also noted that this mutualism was most vulnerable in degraded forest.
Conclusions Hovenia dulcis
peduncle sets are confirmed to adapt primarily to mammalian endozoochory, a mutualistic association similar in function to fleshy pulp or foliage. This demonstrates that plant organ systems can be adapted to unique mutualisms that utilize animal dispersal agents. Such an ecological role has until now been attributed only to bird epizoochory. Future studies should consider more widely the putative role of peduncle sets and mammalian endozoochory as a dispersal mechanism, particularly for those plants that possess relatively large accessory fruits.
doi:10.1093/aob/mct096
PMCID: PMC3690987  PMID: 23644364
Animal dispersal agent; diaspore set; dry-fruited plant; endozoochory; epizoochory; fleshy peduncle; Hovenia dulcis; mutualism; seed dispersal
14.  Variation and evolution of herkogamy in Exochaenium (Gentianaceae): implications for the evolution of distyly 
Annals of Botany  2013;112(1):95-102.
Backgrounds and Aims
The spatial separation of stigmas and anthers (herkogamy) in flowering plants functions to reduce self-pollination and avoid interference between pollen dispersal and receipt. Little is known about the evolutionary relationships among the three main forms of herkogamy – approach, reverse and reciprocal herkogamy (distyly) – or about transitions to and from a non-herkogamous condition. This problem was examined in Exochaenium (Gentianaceae), a genus of African herbs that exhibits considerable variation in floral morphology, including the three forms of herkogamy.
Methods
Using maximum parsimony and maximum likelihood methods, the evolutionary history of herkogamic and non-herkogamic conditions was reconstructed from a molecular phylogeny of 15 species of Exochaenium and four outgroup taxa, based on three chloroplast regions, the nuclear ribosomal internal transcribed spacer (ITS1 and 2) and the 5·8S gene. Ancestral character states were determined and the reconstructions were used to evaluate competing models for the origin of reciprocal herkogamy.
Key results
Reciprocal herkogamy originated once in Exochaenium from an ancestor with approach herkogamy. Reverse herkogamy and the non-herkogamic condition homostyly were derived from heterostyly. Distylous species possessed pendent, slightly zygomorphic flowers, and the single transition to reverse herkogamy was associated with the hawkmoth pollination syndrome. Reductions in flower size characterized three of four independent transitions from reciprocal herkogamy to homostyly.
Conclusions
The results support Lloyd and Webb's model in which distyly originated from an ancestor with approach herkogamy. They also demonstrate the lability of sex organ deployment and implicate pollinators, or their absence, as playing an important role in driving transitions among herkogamic and non-herkogamic conditions.
doi:10.1093/aob/mct097
PMCID: PMC3690988  PMID: 23639954
Distyly; Exochaenium; floral evolution; Gentianaceae; herkogamy; heterostyly; phylogeny
15.  Spatial patterns of photosynthesis in thin- and thick-leaved epiphytic orchids: unravelling C3–CAM plasticity in an organ-compartmented way 
Annals of Botany  2013;112(1):17-29.
Background and Aims
A positive correlation between tissue thickness and crassulacean acid metabolism (CAM) expression has been frequently suggested. Therefore, this study addressed the question of whether water availability modulates photosynthetic plasticity in different organs of two epiphytic orchids with distinct leaf thickness.
Methods
Tissue morphology and photosynthetic mode (C3 and/or CAM) were examined in leaves, pseudobulbs and roots of a thick-leaved (Cattleya walkeriana) and a thin-leaved (Oncidium ‘Aloha’) epiphytic orchid. Morphological features were studied comparing the drought-induced physiological responses observed in each organ after 30 d of either drought or well-watered treatments.
Key Results
Cattleya walkeriana, which is considered a constitutive CAM orchid, displayed a clear drought-induced up-regulation of CAM in its thick leaves but not in its non-leaf organs (pseudobulbs and roots). The set of morphological traits of Cattleya leaves suggested the drought-inducible CAM up-regulation as a possible mechanism of increasing water-use efficiency and carbon economy. Conversely, although belonging to an orchid genus classically considered as performing C3 photosynthesis, Oncidium ‘Aloha’ under drought seemed to express facultative CAM in its roots and pseudobulbs but not in its leaves, indicating that such photosynthetic responses might compensate for the lack of capacity to perform CAM in its thin leaves. Morphological features of Oncidium leaves also indicated lower efficiency in preventing water and CO2 losses, while aerenchyma ducts connecting pseudobulbs and leaves suggested a compartmentalized mechanism of nighttime carboxylation via phosphoenolpyruvate carboxylase (PEPC) (pseudobulbs) and daytime carboxylation via Rubisco (leaves) in drought-exposed Oncidium plants.
Conclusions
Water availability modulated CAM expression in an organ-compartmented manner in both orchids studied. As distinct regions of the same orchid could perform different photosynthetic pathways and variable degrees of CAM expression depending on the water availability, more attention should be addressed to this in future studies concerning the abundance of CAM plants.
doi:10.1093/aob/mct090
PMCID: PMC3690981  PMID: 23618898
Cattleya walkeriana; crassulacean acid metabolism; drought; epiphytic orchid; leaf succulence; non-leaf photosynthesis; Oncidium ‘Aloha’; photosynthetic plasticity
16.  Cotton bracts are adapted to a microenvironment of concentrated CO2 produced by rapid fruit respiration 
Annals of Botany  2013;112(1):31-40.
Background and Aims
Elucidation of the mechanisms by which plants adapt to elevated CO2 is needed; however, most studies of the mechanisms investigated the response of plants adapted to current atmospheric CO2. The rapid respiration rate of cotton (Gossypium hirsutum) fruits (bolls) produces a concentrated CO2 microenvironment around the bolls and bracts. It has been observed that the intercellular CO2 concentration of a whole fruit (bract and boll) ranges from 500 to 1300 µmol mol−1 depending on the irradiance, even in ambient air. Arguably, this CO2 microenvironment has existed for at least 1·1 million years since the appearance of tetraploid cotton. Therefore, it was hypothesized that the mechanisms by which cotton bracts have adapted to elevated CO2 will indicate how plants will adapt to future increased atmospheric CO2 concentration. Specifically, it is hypothesized that with elevated CO2 the capacity to regenerate ribulose-1,5-bisphosphate (RuBP) will increase relative to RuBP carboxylation.
Methods
To test this hypothesis, the morphological and physiological traits of bracts and leaves of cotton were measured, including stomatal density, gas exchange and protein contents.
Key results
Compared with leaves, bracts showed significantly lower stomatal conductance which resulted in a significantly higher water use efficiency. Both gas exchange and protein content showed a significantly greater RuBP regeneration/RuBP carboxylation capacity ratio (Jmax/Vcmax) in bracts than in leaves.
Conclusions
These results agree with the theoretical prediction that adaptation of photosynthesis to elevated CO2 requires increased RuBP regeneration. Cotton bracts are readily available material for studying adaption to elevated CO2.
doi:10.1093/aob/mct091
PMCID: PMC3690982  PMID: 23625144
Bract; cotton; CO2 acclimation; CO2 adaptation; Cyt b6f; Gossypium hirsutum; Jmax/Vcmax; photosynthesis; respiration; Rubisco; stomatal conductance; water use efficiency
17.  High cytokinin levels induce a hypersensitive-like response in tobacco 
Annals of Botany  2013;112(1):41-55.
Background and Aims
Cytokinins are positive regulators of shoot development. However, it has previously been demonstrated that efficient activation of the cytokinin biosynthesis gene ipt can cause necrotic lesions and wilting in tobacco leaves. Some plant pathogens reportedly use their ability to produce cytokinins in disease development. In response to pathogen attacks, plants can trigger a hypersensitive response that rapidly kills cells near the infection site, depriving the pathogen of nutrients and preventing its spread. In this study, a diverse set of processes that link ipt activation to necrotic lesion formation were investigated in order to evaluate the potential of cytokinins as signals and/or mediators in plant defence against pathogens.
Methods
The binary pOp-ipt/LhGR system for dexamethasone-inducible ipt expression was used to increase endogenous cytokinin levels in transgenic tobacco. Changes in the levels of cytokinins and the stress hormones salicylic, jasmonic and abscisic acid following ipt activation were determined by ultra-performance liquid chromatography–electrospray tandem mass spectrometry (UPLC-MS/MS). Trends in hydrogen peroxide content and lipid peroxidation were monitored using the potassium iodide and malondialdehyde assays. The subcellular distribution of hydrogen peroxide was investigated using 3,3′-diaminobenzidine staining. The dynamics of transcripts related to photosynthesis and pathogen response were analysed by reverse transcription followed by quantitative PCR. The effects of cytokinins on photosynthesis were deciphered by analysing changes in chlorophyll fluorescence and leaf gas exchange.
Key Results
Plants can produce sufficiently high levels of cytokinins to trigger fast cell death without any intervening chlorosis – a hallmark of the hypersensitive response. The results suggest that chloroplastic hydrogen peroxide orchestrates the molecular responses underpinning the hypersensitive-like response, including the inhibition of photosynthesis, elevated levels of stress hormones, oxidative membrane damage and stomatal closure.
Conclusions
Necrotic lesion formation triggered by ipt activation closely resembles the hypersensitive response. Cytokinins may thus act as signals and/or mediators in plant defence against pathogen attack.
doi:10.1093/aob/mct092
PMCID: PMC3690983  PMID: 23644362
Cytokinin; hypersensitive response; hydrogen peroxide; lipid peroxidation; pathogenesis-related proteins; salicylic acid; jasmonic acid; abscisic acid; photosynthesis; stomatal conductance; non-photochemical quenching; Nicotiana tabacum
18.  Endogenous cytokinin in developing kiwifruit is implicated in maintaining fruit flesh chlorophyll levels 
Annals of Botany  2013;112(1):57-68.
Background and Aims
Green kiwifruit (Actinidia deliciosa) retain high concentrations of chlorophyll in the fruit flesh, whereas in gold-fleshed kiwifruit (A. chinensis) chlorophyll is degraded to colourless catabolites during fruit development, leaving yellow carotenoids visible. The plant hormone group the cytokinins has been implicated in the delay of senescence, and so the aim of this work was to investigate the link between cytokinin levels in ripening fruit and chlorophyll de-greening.
Methods
The expression of genes related to cytokinin metabolism and signal transduction and the concentration of cytokinin metabolites were measured. The regulation of gene expression was assayed using transient activation of the promoter of STAY-GREEN2 (SGR2) by cytokinin response regulators.
Key Results
While the total amount of cytokinin increased in fruit of both species during maturation and ripening, a high level of expression of two cytokinin biosynthetic gene family members, adenylate isopentenyltransferases, was only detected in green kiwifruit fruit during ripening. Additionally, high levels of O-glucosylated cytokinins were detected only in green kiwifruit, as was the expression of the gene for zeatin O-glucosyltransferase, the enzyme responsible for glucosylating cytokinin into a storage form. Season to season variation in gene expression was seen, and some de-greening of the green kiwifruit fruit occurred in the second season, suggesting environmental effects on the chlorophyll degradation pathway. Two cytokinin-related response regulators, RRA17 and RRB120, showed activity against the promoter of kiwifruit SGR2.
Conclusions
The results show that in kiwifruit, levels of cytokinin increase markedly during fruit ripening, and that cytokinin metabolism is differentially regulated in the fruit of the green and gold species. However, the causal factor(s) associated with the maintenance or loss of chlorophyll in kiwifruit during ripening remains obscure.
doi:10.1093/aob/mct093
PMCID: PMC3690984  PMID: 23644363
Actinidia deliciosa; A. chinensis; chlorophyll degradation; cytokinin; fruit ripening; kiwifruit; STAY-GREEN; transcription factor
19.  Identification and characterization of ten new water gaps in seeds and fruits with physical dormancy and classification of water-gap complexes 
Annals of Botany  2013;112(1):69-84.
Background and Aims
Physical dormancy (PY) occurs in seeds or fruits of 18 angiosperm families and is caused by a water-impermeable palisade cell layer(s) in seed or fruit coats. Prior to germination, the seed or fruit coat of species with PY must become permeable in order to imbibe water. Breaking of PY involves formation of a small opening(s) (water gap) in a morpho-anatomically specialized area in seeds or fruits known as the water-gap complex. Twelve different water-gap regions in seven families have previously been characterized. However, the water-gap regions had not been characterized in Cucurbitaceae; clade Cladrastis of Fabaceae; subfamilies Bombacoideae, Brownlowioideae and Bythnerioideae of Malvaceae; Nelumbonaceae; subfamily Sapindoideae of Sapindaceae; Rhamnaceae; or Surianaceae. The primary aims of this study were to identify and describe the water gaps of these taxa and to classify all the known water-gap regions based on their morpho-anatomical features.
Methods
Physical dormancy in 15 species was broken by exposing seeds or fruits to wet or dry heat under laboratory conditions. Water-gap regions of fruits and seeds were identified and characterized by use of microtome sectioning, light microscopy, scanning electron microscopy, dye tracking and blocking experiments.
Key Results
Ten new water-gap regions were identified in seven different families, and two previously hypothesized regions were confirmed. Water-gap complexes consist of (1) an opening that forms after PY is broken; (2) a specialized structure that occludes the gap; and (3) associated specialized tissues. In some species, more than one opening is involved in the initial imbibition of water.
Conclusions
Based on morpho-anatomical features, three basic water-gap complexes (Types-I, -II and -III) were identified in species with PY in 16 families. Depending on the number of openings involved in initial imbibition, the water-gap complexes were sub-divided into simple and compound. The proposed classification system enables understanding of the relationships between the water-gap complexes of taxonomically unrelated species with PY.
doi:10.1093/aob/mct094
PMCID: PMC3690985  PMID: 23649182
Chalaza; dye tracking; fruit coat; hilum; micropyle; palisade cells; physical dormancy; PY breaking; seed coat; water-gap complex
20.  Nodule morphology, symbiotic specificity and association with unusual rhizobia are distinguishing features of the genus Listia within the southern African crotalarioid clade Lotononis s.l. 
Annals of Botany  2013;112(1):1-15.
Background and Aims
The legume clade Lotononis sensu lato (s.l.; tribe Crotalarieae) comprises three genera: Listia, Leobordea and Lotononis sensu stricto (s.s.). Listia species are symbiotically specific and form lupinoid nodules with rhizobial species of Methylobacterium and Microvirga. This work investigated whether these symbiotic traits were confined to Listia by determining the ability of rhizobial strains isolated from species of Lotononis s.l. to nodulate Listia, Leobordea and Lotononis s.s. hosts and by examining the morphology and structure of the resulting nodules.
Methods
Rhizobia were characterized by sequencing their 16S rRNA and nodA genes. Nodulation and N2 fixation on eight taxonomically diverse Lotononis s.l. species were determined in glasshouse trials. Nodules of all hosts, and the process of infection and nodule initiation in Listia angolensis and Listia bainesii, were examined by light microscopy.
Key Results
Rhizobia associated with Lotononis s.l. were phylogenetically diverse. Leobordea and Lotononis s.s. isolates were most closely related to Bradyrhizobium spp., Ensifer meliloti, Mesorhizobium tianshanense and Methylobacterium nodulans. Listia angolensis formed effective nodules only with species of Microvirga. Listia bainesii nodulated only with pigmented Methylobacterium. Five lineages of nodA were found. Listia angolensis and L. bainesii formed lupinoid nodules, whereas nodules of Leobordea and Lotononis s.s. species were indeterminate. All effective nodules contained uniformly infected central tissue. Listia angolensis and L. bainesii nodule initials occurred on the border of the hypocotyl and along the tap root, and nodule primordia developed in the outer cortical layer. Neither root hair curling nor infection threads were seen.
Conclusions
Two specificity groups occur within Lotononis s.l.: Listia species are symbiotically specific, while species of Leobordea and Lotononis s.s. are generally promiscuous and interact with rhizobia of diverse chromosomal and symbiotic lineages. The seasonally waterlogged habitat of Listia species may favour the development of symbiotic specificity.
doi:10.1093/aob/mct095
PMCID: PMC3690986  PMID: 23712451
Crotalarieae; Lotononis s.l.; Listia; Leobordea; nodulation; nodule structure; symbiotic specificity; rhizobia; Methylobacterium; Microvirga
21.  MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions 
Annals of Botany  2013;112(1):103-114.
Background and Aims
Root hydrotropism is a response to water-potential gradients that makes roots bend towards areas of higher water potential. The gene MIZU-KUSSEI1 (MIZ1) that is essential for hydrotropism in Arabidopsis roots has previously been identified. However, the role of root hydrotropism in plant growth and survival under natural conditions has not yet been proven. This study assessed how hydrotropic response contributes to drought avoidance in nature.
Methods
An experimental system was established for the study of Arabidopsis hydrotropism in soil. Characteristics of hydrotropism were analysed by comparing the responses of the miz1 mutant, transgenic plants overexpressing MIZ1 (MIZ1OE) and wild-type plants.
Key Results
Wild-type plants developed root systems in regions with higher water potential, whereas the roots of miz1 mutant plants did not show a similar response. This pattern of root distribution induced by hydrotropism was more pronounced in MIZ1OE plants than in wild-type plants. In addition, shoot biomass and the number of plants that survived under drought conditions were much greater in MIZ1OE plants.
Conclusions
These results show that hydrotropism plays an important role in root system development in soil and contributes to drought avoidance, which results in a greater yield and plant survival under water-limited conditions. The results also show that MIZ1 overexpression can be used for improving plant productivity in arid areas.
doi:10.1093/aob/mct098
PMCID: PMC3690989  PMID: 23658369
Arabidopsis thaliana; drought avoidance; hydrotropism; root system; MIZU-KUSSEI1 (MIZ1)
22.  Strigolactones activate different hormonal pathways for regulation of root development in response to phosphate growth conditions 
Annals of Botany  2012;112(2):409-415.
Background
Strigolactones (SLs) – a group of plant hormones and their derivatives – have been found to play a role in the regulation of root development, in addition to their role in suppression of lateral shoot branching: they alter root architecture and affect root-hair elongation, and SL signalling is necessary for the root response to low phosphate (Pi) conditions. These effects of SLs have been shown to be associated with differential activation of the auxin and ethylene signalling pathways.
Scope
The present review highlights recent findings on the activity of SLs as regulators of root development, in particular in response to low Pi stress, and discusses the different hormonal networks putatively acting with SLs in the root's Pi response.
Conclusions
SLs are suggested to be key regulators of the adaptive responses to low Pi in the root by modulating the balance between auxin and ethylene signalling. Consequently, they impact different developmental programmes responsible for the changes in root system architecture under differential Pi supply.
doi:10.1093/aob/mcs216
PMCID: PMC3698373  PMID: 23059852
Strigolactones; root; phosphate; hormones; ethylene; auxin; root hairs; primary root; lateral root
23.  A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI) 
Annals of Botany  2012;112(2):297-316.
Background
Agriculture is the single largest geo-engineering initiative that humans have initiated on planet Earth, largely through the introduction of unprecedented amounts of reactive nitrogen (N) into ecosystems. A major portion of this reactive N applied as fertilizer leaks into the environment in massive amounts, with cascading negative effects on ecosystem health and function. Natural ecosystems utilize many of the multiple pathways in the N cycle to regulate N flow. In contrast, the massive amounts of N currently applied to agricultural systems cycle primarily through the nitrification pathway, a single inefficient route that channels much of this reactive N into the environment. This is largely due to the rapid nitrifying soil environment of present-day agricultural systems.
Scope
In this Viewpoint paper, the importance of regulating nitrification as a strategy to minimize N leakage and to improve N-use efficiency (NUE) in agricultural systems is highlighted. The ability to suppress soil nitrification by the release of nitrification inhibitors from plant roots is termed ‘biological nitrification inhibition’ (BNI), an active plant-mediated natural function that can limit the amount of N cycling via the nitrification pathway. The development of a bioassay using luminescent Nitrosomonas to quantify nitrification inhibitory activity from roots has facilitated the characterization of BNI function. Release of BNIs from roots is a tightly regulated physiological process, with extensive genetic variability found in selected crops and pasture grasses. Here, the current status of understanding of the BNI function is reviewed using Brachiaria forage grasses, wheat and sorghum to illustrate how BNI function can be utilized for achieving low-nitrifying agricultural systems. A fundamental shift towards ammonium (NH4+)-dominated agricultural systems could be achieved by using crops and pastures with high BNI capacities. When viewed from an agricultural and environmental perspective, the BNI function in plants could potentially have a large influence on biogeochemical cycling and closure of the N loop in crop–livestock systems.
doi:10.1093/aob/mcs230
PMCID: PMC3698375  PMID: 23118123
AMO; ammonia mono-oxygenase; biological nitrification inhibition; BNI; BNI capacity; brachialactone; fatty acids; HAO; hydroxylamine oxidoreductase; high-nitrifying production systems; low-nitrifying production systems; nitrification; Nitrosomonas; nitrate leaching; synthetic nitrification inhibitors; nitrous oxide emissions; sustainability
24.  A conceptual model of root hair ideotypes for future agricultural environments: what combination of traits should be targeted to cope with limited P availability? 
Annals of Botany  2012;112(2):317-330.
Background
Phosphorus (P) often limits crop production and is frequently applied as fertilizer; however, supplies of quality rock phosphate for fertilizer production are diminishing. Plants have evolved many mechanisms to increase their P acquisition, and an understanding of these traits could result in improved long-term sustainability of agriculture. This Viewpoint focuses on the potential benefits of root hairs to sustainable production.
Scope
First the various root-related traits that could be deployed to improve agricultural sustainability are catalogued, and their potential costs and benefits to the plant are discussed. A novel mathematical model describing the effects of length, density and longevity of root hairs on P acquisition is developed, and the relative benefits of these three root-hair traits to plant P nutrition are calculated. Insights from this model are combined with experimental data to assess the relative benefits of a range of root hair ideotypes for sustainability of agriculture.
Conclusions
A cost–benefit analysis of root traits suggests that root hairs have the greatest potential for P acquisition relative to their cost of production. The novel modelling of root hair development indicates that the greatest gains in P-uptake efficiency are likely to be made through increased length and longevity of root hairs rather than by increasing their density. Synthesizing this information with that from published experiments we formulate six potential ideotypes to improve crop P acquisition. These combine appropriate root hair phenotypes with architectural, anatomical and biochemical traits, such that more root-hair zones are produced in surface soils, where P resources are found, on roots which are metabolically cheap to construct and maintain, and that release more P-mobilizing exudates. These ideotypes could be used to inform breeding programmes to enhance agricultural sustainability.
doi:10.1093/aob/mcs231
PMCID: PMC3698376  PMID: 23172412
Arabidopsis; barley; Hordeum vulgare; cost/benefit; modelling; phosphorus; root architecture; root anatomy; root function; root hairs
25.  Use of genotype × environment interactions to understand rooting depth and the ability of wheat to penetrate hard soils 
Annals of Botany  2012;112(2):359-368.
Background
Root systems are well-recognized as complex and a variety of traits have been identified as contributing to plant adaptation to the environment. A significant proportion of soil in south-western Australia is prone to the formation of hardpans of compacted soil that limit root exploration and thus access to nutrients and water for plant growth. Genotypic variation has been reported for root-penetration ability of wheat in controlled conditions, which has been related to field performance in these environments. However, research on root traits in field soil is recognized as difficult and labour intensive. Pattern analysis of genotype × environment (G × E) interactions is one approach that enables interpretation of these complex relationships, particularly when undertaken with probe genotypes with well-documented traits, in this case, for the ability to penetrate a wax layer. While the analytical approach is well-established in the scientific literature, there are very few examples of pattern analysis for G × E interactions applied to root traits of cereal crops.
Scope
In this viewpoint, we aim to review the approach of pattern analysis for G × E interaction and the importance of environment and genotype characterization, with a focus on root traits. We draw on our research on G × E interaction for root depth and related studies on genotypic evaluation for root-penetration ability. In doing so, we wish to explore how pattern analysis can aid in the interpretation of complex root traits and their interaction with the environment and how this may explain patterns of adaptation and inform future research.
Conclusions
With appropriate characterization of environments and genotypes, the G × E approach can be used to aid in the interpretation of the complex interactions of root systems with the environment, inform future research and therefore provide supporting evidence for selecting specific root traits for target environments in a crop breeding programme.
doi:10.1093/aob/mcs251
PMCID: PMC3698378  PMID: 23204508
Hardpan; wax layer; Western Australia; pattern analysis; wheat; Triticum aestivum

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