Fruits come in an impressive array of shapes, sizes, and consistencies, and also display a huge diversity in biochemical/metabolite profiles, wherein lies their value as rich sources of food, nutrition, and pharmaceuticals. This is in addition to their fundamental function in supporting and dispersing the developing and mature seeds for the next generation.
Understanding developmental processes such as fruit development and ripening, particularly at the genetic level, was once largely restricted to model and crop systems for practical and commercial reasons, but with the expansion of developmental genetic and evo-devo tools/analyses we can now investigate and compare aspects of fruit development in species spanning the angiosperms. We can superimpose recent genetic discoveries onto the detailed characterization of fruit development and ripening conducted with primary considerations such as yield and harvesting efficiency in mind, as well as on the detailed description of taxonomically relevant characters.
This free review article focuses on two very morphologically distinct and evolutionary distant fruits: the capsule of opium poppy, and the grain or caryopsis of cereals. Both are of massive economic value, but because of very different constituents; alkaloids of varied pharmaceutical value derived from secondary metabolism in opium poppy capsules, and calorific energy fuel derived from primary metabolism in cereal grains. Through comparative analyses in these and other fruit types, interesting patterns of regulatory gene function diversification and conservation are beginning to emerge.
Sofia Kourmpetli and Sinéad Drea. The fruit, the whole fruit, and everything about the fruit. J Exp Bot. Apr 10 2014.
Image: Ryan Kitko/Wikimedia Commons.
Unusually for this column (why give the ‘competition’ a free bit of publicity, after all?), I here wish to promote The Scientist magazine. As a general science news item site it occasionally features plant-related items, but it has surpassed itself with its 1st January 2014 collection. Not only does it feature a wonderful image of the fruit of the lotus plant on its cover, but it also contains four big plant articles(!).
By way of introducing that compilation, Mary Aberlin observes in her editorial that, ‘the panoply of fictional plants offers a large and varied dose of the weird and wonderful. But there’s no need to resort to fiction to find truly unusual plant characteristics’… so, read on! Accordingly, the selection comprises an item by Abby Olena that considers halotropism, a newly identified tropism in roots. This showcases a study by Carlos Galvan-Ampudia et al. that demonstrates active growth of roots of several plant species away from sites of high salt content, and which is not gravitropism. This work begs the question of how many other tropisms might still await discovery in that understudied plant organ.
In ‘Green gold’ Tracy Vence reports on the discovery of gold bioaccumulation in eucalyptus leaves, which was covered on this very blog not so long ago. Megan Scudellari’s article begins by posing the question, ‘What do cells, genes, mutations, transposons, RNA silencing, and DNA recombination have in common?’: the answer – but, of course! – is that all were first discovered in plants; she then considers how plant DNA is challenging preconceptions about the evolution of life (including our own species). And Dan Cossins considers the question of whether plants ‘talk’ to each other. Reviewing a wide-ranging body of work, the conclusion is that plants do communicate and interact with each other, both above and below ground, in surprisingly subtle and sophisticated ways. And by way of demonstrating how the time is right for certain ideas, Kat McGowan has an item in Quanta Magazine on ‘The secret language of plants’. Almost inevitably these sorts of articles raise the spectre of how intelligent plants are, and that issue is given a good airing in Michael Pollan’s New Yorker article. What a great botanical start to the New Year (which traditionally starts on 10th April…)!
[Visit YouTube for a documentary on plant intelligence, and also if you want to know what plants talk about – Ed.]
Pseudomonas syringae is a widespread bacterial pathogen that causes disease on a broad range of economically important plant species. In order to infect, P. syringae produces a number of toxins and uses a type III secretion system to deliver effector proteins into eukaryotic cells. This mechanism is essential for successful infection by both plant- and animal-associated bacteria as bacterial mutants are no longer pathogenic. However, the molecular function and host targets of the vast majority of effectors remain largely unknown.
Plant immunity relies on a complex network of small-molecule hormone signaling pathways (see: Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of botany, 100(4), 681-697). Classically, salicylic acid (SA) signaling mediates resistance against biotrophic and hemi-biotrophic microbes such as P. syringae, whereas a combination of jasmonic acid (JA) and ethylene (ET) pathways activates resistance against necrotrophs such as the fungus Botrytis cinerea. SA and JA/ET defense pathways generally antagonize each other – elevated resistance against biotrophs is often correlated with increased susceptibility to necrotrophs and vice versa. The collective contribution of these two hormones during plant-pathogen interactions is crucial to the success of the interaction. Remarkably, some Pseudomonas strains have evolved a sophisticated strategy for manipulating hormonal balance by producing the toxin coronatine (COR), which mimics the plant hormone jasmonate-isoleucine (JA-Ile). The JA-Ile pathway plays a key role in plant immunity by activating defenses against fungal pathogens, while promoting bacterial growth by inhibiting the salicylic acid (SA)-dependent defenses required for Pseudomonas resistance.
A recent paper in PLOS Biology reports that the effector HopX1 from a Pseudomonas syringae strain that does not produce COR exploits an alternative evolutionary strategy to activate the JA-Ile pathway. HopX1 encodes a cysteine protease that interacts with and promotes the degradation of key JA pathway repressors, the JAZ proteins. Correspondingly, ectopically expressing HopX1 in the model plant Arabidopsis induces the expression of JA-dependent genes, and natural infection with Pseudomonas producing HopX1 promotes bacterial growth in a similar fashion to COR. These results highlight a novel example by which a bacterial effector directly manipulates core regulators of hormone signaling to facilitate infection:
Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, et al. (2014) The Bacterial Effector HopX1 Targets JAZ Transcriptional Repressors to Activate Jasmonate Signaling and Promote Infection in Arabidopsis. PLoS Biol 12(2): e1001792. doi:10.1371/journal.pbio.1001792
Image: Mariana Ruiz Villarreal/Wikimedia Commons.
Plants are remarkably sensitive to their environment, responding by appropriate growth and development to a wide range of environmental stimuli. In the case of gravity, the appropriate response is for stems to grow upwards (‘away from the source of gravity’; negative geotropism), and for roots to grow downwards (‘towards the source of gravity’; positive geotropism – for examples, see reviews by Elison Blancaflor and Patrick Masson and by Miyo Morita). Although the details of the full pathway involved are still the subject of intense research efforts, a role for gravity-stimulated repositioning of cell-located statoliths (starch-bearing amyloplasts) in the gravity-detection side of things has long been proposed. However, the dynamic – rather than settled – nature of such amyloplasts has cast doubt on their effectiveness to act in this way. Now, elegant work by Masatsugu Toyota et al. has demonstrated that amyloplast displacement is necessary for gravisensing (in arabidopsis shoots). Using a custom-built centrifuge microscope they show that ‘sedimentary movements of amyloplasts under hypergravity conditions are linearly correlated with gravitropic curvature in wild-type stems’. Furthermore, and using a range of gravitropic mutants that do not exhibit a normal response under the Earth’s usual 1 g gravity field, they demonstrate that their ‘hypergravity-induced amyloplast sedimentation and gravitropic curvature… was identical to that of wild-type plants’. Such work supports the view that arabidopsis shoots do have a gravisensing mechanism that converts the number of gravity-settling amyloplasts into gravitropic signals. And restoration of the gravitropic response by hypergravity in the gravitropic mutants examined indicates that those plants probably also have a functional gravisensing mechanism, albeit one that is not triggered at 1 g. Nice work. But in view of recent upsets (see previous ‘Ouch! That must hurt…’ post), I wonder if it also applies to non-arabidopsis plants…? Still, it is good to have the odd positive story about arabidopsis (I suppose…!).
[For more on the tangled web that is plant gravity-sensing and involvement of the actin cytoskeleton, check out the recent review by Elison Blancaflor – Ed.]
Image: Taro Taylor/Wikimedia Commons.
It’s a tribute to the fantasticness of plants – and photosynthesis in particular – that even animals want to be like them. Arguably, none more so than some sea slugs, which for many millennia have eaten seaweeds and integrated their chloroplasts into their bodies (a phenomenon known as kleptoplasty). The assumption that underlies such acquisitive behaviour is that the new owners use those sequestered verdant powerhouses as a fuel source for their own purposes. A lovely idea – and one that will have found its way into the textbooks, and featured in lectures based thereon. But! Gregor Christa et al. have concluded that, while such ‘stolen plastids’ display light-dependent CO2 fixation (i.e. photosynthesis), light is not essential for the studied sea slugs – Elysia timida and Plakobranchus ocellatus – to stave off starvation. Indeed, they conclude that the internalized plastids seem to be a slowly digested food source rather than a source of solar power. In other words, this is an example of plants feeding the planet (again!). However, another bonus of this work is that animals are still just animals and not proxy plants. Which is good, because, to paraphrase one Harold Woolhouse, if one wants to understand the biology of plants one will ultimately have to work on… plants.
[However, if you wish to study animals that penetrate each other in the head during sex, then that’s where sea slugs really come into their own. But if you want more on photosynthetic animals, check out this article by Sarah Rybak – Ed.]
Image: Britton & Brown. 1913. An illustrated flora of the northern United States, Canada and the British Possessions. Charles Scribner’s Sons, New York.
Schadenfreude (taking pleasure in the misfortunes of others) is not the most attractive of human traits, but it can be so satisfying. And I bet there’s more than a little of that throughout the world occasioned by the discovery that the model plant Arabidopsis thaliana seems not to be such a good model after all. And the reason for this global wave of ‘arabidisenchantia’ relates to a rather fundamental property of cells known as nonsense-mediated mRNA decay (NMD). NMD is a so-called surveillance pathway that reduces errors in gene expression by eliminating aberrant m(essenger)RNAs that would otherwise encode incomplete polypeptides. Important though this process is for cell survival, it had been assumed that plants used it in a different way to animals because a gene for a key protein – SMG1 (phosphatidylinositol 3-kinase-related kinase) – in the pathway had not been identified in Arabidopsis thaliana (afka* ‘the universal plant’), nor in fungi. However, and thanks to iconoclastic (albeit probably unintentionally) work by James Lloyd and Brendan Davies, we [arabothalocentric plant biologists and those who needs must rely on their abundantly-funded researches - which is pretty much all of the rest of us...] can all sleep more soundly in our beds. They show that SMG1 – the gene that codes for SMG1 – is not animal-specific, but is found ‘in a range of eukaryotes, including all examined green plants [my emphasis] with the exception of A. thaliana’. The misconception about the importance of SMG1 in plants appears to have arisen because the gene was lost from A. thaliana ’s genome 5–10 millions of years ago. Interestingly, SMG1 is found in the genome of the closely related A. lyrata… So, A. thaliana is unique after all(!), though not in quite the way its promoters (pun intended…?) might have liked. But if thale cress has carelessly lost this gene, what else has it lost (but which may have been retained by more typical plants)…? I predict more Arabidopsis applecart-upsetting in the future…
* afka = as formerly known as…
Image: Robert A. Rohde/Wikimedia Commons.
Many abiotic variables affect plants, e.g. levels of light, carbon dioxide and water. One of the most important of those non-biotic factors is temperature. Now, given its importance you could be forgiven for assuming that it is recorded accurately and correctly. Unfortunately, that isn’t always the case. Take for instance the temperature of the meristem (symbolised as Tmeristem), which is important in driving plant development. For such a crucial aspect of plant biology studies have largely relied on measuring the temperature of the air surrounding the plant (Tair). Tair is measured because it is assumed to represent the meristem temperature because plants are poikilotherms (organisms whose ‘internal temperature varies considerably … Usually the variation is a consequence of variation in the ambient environmental temperature’). Whilst that assumption may seem reasonable – and it does save the would-be investigator the trouble of penetrating the umpteen layers of developing leaves, etc, that may sheathe the apical meristem, it is nonetheless an assumption. And the veracity of assumptions must be tested, which is what Andreas Savvides et al. did. Guess what they found! That’s right: Tmeristem differed from Tair – ranging between –2.6 and 3.8 °C in tomato, and –4.1 and 3.0 °C in cucumber(!). As the team conclude, ‘for properly linking growth and development of plants to temperature… Tmeristem should be used instead of Tair’.
If you’re now intrigued by detecting temperatures within cells, you might like to explore the nanoscale thermometer developed by G. Kucsko et al. Using ‘quantum manipulation of nitrogen vacancy (NV) colour centres in diamond nanocrystals’ it can detect temperature variations as small as 44 mK(!) and can measure the local thermal environment at length scales as low as 200 nm(!!). Or, if you want a more biological approach, check out the genetically encoded sensor that fuses green fluorescent protein to a thermosensing protein derived from Salmonella, as showcased by Shigeki Kiyonaka et al. Although proof of this particular principle was demonstrated with thermogenesis in the iconic mitochondria of brown adipocytes (and the somewhat less iconic endoplasmic reticulum of myotubes), the team envisage it could be used to investigate this phenomenon in other living cells. Maybe even within the cone cells of tropical cycads that undergo impressive increases in temperature, where Tcone can be markedly greater that Tair. In view of concerns about global temperature changes and effects of temperature on regulation of such economically important processes as flowering, accurate temperature information in planta – and an appreciation of the temperature that plants are actually responding to – is likely to become increasingly important.
[For a useful set of slides summarising Savvides et al.’s work, visit slideshare.net. For a less physics-oriented interpretation of the Nature nanoscale thermometry article try the accompanying ‘News and Views’ item by Konstantin Sokolov – Ed.].
Image: David Iliff/Wikimedia Commons (CC-BY-SA 3.0).
OK, I know, this item is the real ‘money doesn’t grow on trees’ story you were expecting. So, I’ll try not to disappoint. Melvyn Lintern et al. provide the first evidence of particulate gold (Au) within natural – i.e. not from laboratory experimentation (and therefore which evidence doesn’t count..?) – specimens of living biological tissue. The living biological tissue in question is that of the iconic Australian plant species eucalyptus, the gum tree. Apparently, and hitherto, reports of Au from plant samples have led to questions as to whether the Au was within the tissues (and therefore absorbed) or adsorbed onto the external surfaces as a result of aerial contamination. The team consider their discovery to demonstrate active biogeochemical absorption of Au, and it may therefore be used as a sort of bioassay (quite how quantitative this is may require further testing – maybe even experimentation…) to indicate the presence of soil-based Au deposits within the reach of the tree’s roots (the presumed route for uptake of the metal from the soil). The overall effect of this study is a little spoilt by the final sentence of the abstract, which begins, ‘This observation conclusively demonstrates active biogeochemical adsorption of Au…’. Shouldn’t that ante-penultimate word be absorption? Potential use of plants as agents to absorb metals – and other compounds – from soils and waters has been widely touted as a method for cleaning up such environments and comes under the broad category of phytoremediation. However, the fact that some plants may accumulate economically important metals – such as gold – has long been recognised and underlies the practice of geobotanical prospecting, which apparently dates as far back as the 5th century BCE in China. Whilst this study isn’t necessarily proposing use of eucalyptus in a bioindicator capacity, the authors do suggest that the gold therein might be extractable on a commercial basis. For more on this topic, see Sheoran et al.’s articles on ‘phytomining’ in general and of that for gold in particular. Anyway, I think somebody’s missing a trick here. What’s the iconic Australian animal species? The herbivorous koala, which famously has a diet rich in leaves of… eucalyptus. Now, applying the well-known principle of biomagnification – whereby organisms higher up the food chain accumulate materials from what they feed on – if koalas can be persuaded to eat only Au-loaded gum-tree leaves, then maybe their faecal pellets may contain gold, but concentrated to much higher levels than those found within their food source. Just a little nugget (!) of information I’m happy to share. All somebody needs to do is harvest the stuff (but isn’t that why postgrads/postdocs were invented..?). What’s that you say, where there’s muck there’s brass? Indeed! After all, we all know how expensive coffee is when made from the ‘beans’ that have been peristaltically massaged and ‘processed’ by passage through the alimentary tract of the Asian palm civet! And in a more scientifically imaginative – though similarly scatologically-inclined – ‘muck = brass’ way the veracity in this wise saying is verified by work in Australia’s antipodean neighbour, New Zealand. Exhibit A, the evidence base that is the coprolite (‘fossilized feces’) recently exploited by Jamie Wood et al. [http://dx.doi.org/10.1073/pnas.1307700110] to discern information about the ecology of four sympatric (species living in the same geographical area) species of moa – flightless herbivorous birds, which became extinct in New Zealand about 600 years ago. Unfortunately, there’s insufficient space for the details of the study here, but it involves identification of vegetation from pollen, aDNA (ancient DNA), and plant macrofossils within the bird droppings (and therefore inferences about moas’ diet and habitat). This is a great example of that admirable ‘rolling-up-your-shirt-sleeves-and-getting-your-hands-dirty’ dedication to the cause of true science; definitely not merely going through the motions(!). What, after all, is more valuable than brass, or even gold? Knowledge! Well, some sorts of knowledge anyway, because, and rather vaguely, the Antipodean team’s ‘golden gum tree’ article just mentions ‘Eucalyptus trees’; there’s no further taxonomic help to their identity in the Supplementary Information either. So, although the article itself is Open Access, maybe naming the species concerned is too commercially sensitive for general consumption?
Image: Wikimedia Commons.
It’s a little naughty to consider these two elements together, I know, because this may unintentionally add to the confusion that often ensues in class when you ask students to tell you the full chemical names for elements with the symbol P – phosphorus – and K – potassium. Oh, the near-Pavlovian, knee-jerk temptation for them to say potassium for P (but not nearly as annoying as those who spell phosphorus with an additional ‘o’ – phosphorous…). Anyway, and since there is so much out there in the cybersphere dealing with phosphorus, I will only flag up Professor John Raven’s typically thoughtful review of the evolution of autotrophy (‘self-feeding’, e.g. photosynthesis, but not restricted to that plant-like process) in relation to requirement for P, ‘the ultimate elemental resource limiting biological productivity through Earth’s history’. Written to redress a perceived imbalance in emphasis that has hitherto concentrated on the roles of C, N and Fe in the evolution of autotrophy and right that historical wrong, Raven’s review ranges widely, from the origins of life, to the roles of P in organisms, PUE (phosphorus use efficiency), to growth-limitation via an effect on water use efficiency (WUE) from P insufficiency.
The K contribution is a consideration of the so-called potassium paradox. For many years K has been added – in the form of KCl – to soils as a fertiliser in efforts to improve agricultural productivity of corn and other grain crops (despite K being one of the most abundant elements in the earth’s crust and being more readily available than N, P or S…). Indeed, so universal is the presumption that K is needed that artificial fertilisers are typically defined by their NPK rating, because K is usually added along with the major plant-growth-limiting nutrients N and P. A study by Saeed Khan et al. has questioned the basis of traditional tests to detect K soil levels – and hence the justification for additional inputs thereof – and even the need for K fertilisation at all. Indeed, their work showed instances of an increase in soil K level in the absence of artificial inputs – ascribed to return of K from plant residues to the soil. Furthermore, their extensive survey of more than 2100 yield-response trials confirmed that not only is KCl addition unlikely to increase crop yield, but – in more than 1400 instances – such K fertilisation actually led to a ‘detrimental effect… on the quality of major food, feed and fiber crops, with serious implications for soil productivity and human health’. As the authors explained, ‘Potassium depresses calcium and magnesium, which are beneficial minerals for any living system’; for example, diets low in Ca can also trigger human diseases such as osteoporosis, rickets and colon cancer. Another major human health concern arises from the chloride in the KCl, which mobilises Cd (cadmium) in the soil and promotes accumulation of this heavy metal in cereals. A paradoxical situation, indeed!
[Ed. - for more on the nutritional complexities and intricacies of phosphorus, try Prof. Raven's recent Frontiers in Plant Science article entitled "RNA function and phosphorus use by photosynthetic organisms".]