On the Inside

Arbuscular mycorrhizal fungi (AMF) inhabit the soils of virtually all terrestrial ecosystems, forming symbiotic associations with most plants. The host plants incur substantial carbon costs to sustain this symbiosis, but in return, they obtain multiple benefits from the fungal partners, most importantly the provision of mineral nutrients. AMF may supply up to 90% of the host plant’s nitrogen and phosphorus requirements. Typically, AMF exhibit little host specificity; a single individual may form a common mycorrhizal network (CMN) between several coexisting plant individuals, even from different species. Such CMNs may be enlarged through hyphal fusion of conspecific AMF. The functionality of CMNs formed by the fusion of two individual fungal networks by hyphal anastomoses has been demonstrated by tracing nutrient allocation between individual host plants upon fusion of their associated CMNs. Little is known about the terms of trade in such CMNs between plants and their shared fungal partners. To address this question, Walder et al. (pp. 789–797) set up microcosms containing a pair of test plants, interlinked by a CMN of Glomus intraradices or Glomus mosseae. The plants studied were flax (Linum usitatissimum), a C3 plant, and sorghum (Sorghum bicolor), a C4 plant. C3 and C4 plants display distinctly different 13C/12C isotope compositions. These properties allowed the authors to differentially assess the carbon investment of the two plants into the CMN through stable isotope tracing. In parallel, the authors determined the “return of investment” of the plants, i.e. the acquisition of nutrients via CMN, using 15N and 33P as tracers. Depending on the AMF species, they found a strong asymmetry in the terms of trade: Flax invested little carbon but gained up to 94% of the nitrogen and phosphorus provided by the CMN. This exchange highly facilitated the growth of flax. In contrast, sorghum invested massive amounts of carbon, and growth was barely affected. Overall, biomass production in the mixed culture surpassed the mean of the two monocultures. Thus, CMNs may contribute to interplant facilitation and the boosts in productivity often found with intercropping compared with conventional monocropping. Plants are immune to most potential pathogens (nonhost disease resistance) and have the ability to reduce the disease severity of actual pathogens (basal disease resistance). Both forms of resistance are initiated by the recognition of the (potential) pathogens by way of chemical cues called microbial-associated molecular patterns (MAMPs). Pattern recognition receptors at the cell surface perceive MAMPs and initiate the immune response. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating the FLS2-mediated signaling remain largely unknown. Frei dit Frey et al. (pp. 798–809) show that the plasma membrane calcium (Ca2+) ATPase ACA8 forms a complex with FLS2 in planta. ACA8 and ACA10 belong to the family of type 2B autoinhibited Ca2+ ATPases consisting of 10 members in Arabidopsis. ACA8, ACA9, and ACA10 group into a distinct subfamily and accumulate at the plasma membrane, whereas ACA9 expression is restricted to pollen. ACA8 and ACA10 are expressed throughout the plant and have not yet been assigned any specific function besides inflorescence growth. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many downstream responses, such as the generation of reactive oxygen species and the transcriptional activation of defense-associated genes. Mutant aca8/aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas Ca2+-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results suggest that the MAMP-induced Ca2+ burst is required for proper transcriptional reprogramming upon elicitation. The volatile composition of strawberry (Fragaria × ananassa) fruits has been extensively studied, and more than 360 constituents have been reported, including esters, aldehydes, ketones, alcohols, terpenes, furanones, and sulfur compounds. However, only 20 or so of these compounds, including mesifurane, which adds a burnt sherry-like flavor, contribute to the flavor and aroma of strawberry fruits. To investigate genetic factors controlling strawberry flavor, Zorrilla-Fontanesi et al. (pp. 851–870) profiled volatile compounds released from two strawberry populations: one flavorful, the other less so. More than 300 volatile compounds were detected, of which 87 were identified by comparison of mass spectrum and retention time to those of pure standards. The especially flavorful population produced higher volatile levels. Cluster analysis grouped the volatiles into distinct chemically related families and revealed a complex metabolic network underlying volatile production in strawberry fruit. Seventy quantitative trait loci covering 48 different volatiles were detected, with several of them remaining stable over time and mapped as major quantitative trait loci. Loci controlling γ-decalactone and mesifurane content were mapped as qualitative traits. The authors show that one homeolog of the O-methyltransferase gene (FaOMT) is the locus responsible for the natural variation of mesifurane content. Readers interested in the roles of O-methyltransferases in secondary compound production may also find of interest a contribution by Dang and Facchini (pp. 618–631) concerning the role of three O-methyltransferases involved in the biosynthesis of noscapine (a cough-suppressing alkaloid) in opium poppy (Papaver somniferum). Many plants are especially vulnerable to cold stress at the reproductive growth stage. Recently, the molecular basis underlying the developmental responses of the anther to environmental stresses has been a subject of intense research. The male sterility of thermosensitive genic male sterile (TGMS) lines of wheat (Triticum aestivum) is strictly controlled by temperature. The early phase of anther development is especially susceptible to cold stress. MicroRNAs play an important role in plant development and in responses to environmental stress. By comparing the expression profiles of small RNAs (smRNAs) and their targets, Tang et al. (pp. 721–738) have determined that smRNAs involved in the auxin signaling pathway may play a significant and specific role in the plant response to cold stress during spike development in the TGMS line. The results of their studies suggest that changes in the abundance of these cold stress-responsive smRNAs mediate the abnormal activity of target ARFs (for Auxin-Responsive Factors) that are important for anther development, thereby causing male sterility of the TGMS line under cold conditions. Multicellular eukaryotes demonstrate nongenetic, heritable phenotypic versatility in their adaptation to environmental changes. This form of inheritance is comprised of interacting epigenetic, maternal, and environmental factors. Maternal effects, as yet unidentified, can have a pronounced influence on plant phenotypic adaptation to changing environmental conditions. Although maternal effects have been shown to influence plant responses, the involvement of organellar processes in maternal inheritance has not been demonstrated. To explore the control of phenotypy in higher plants, Xu et al. (pp. 710–720) examined the effect of a single nuclear gene, MutS HOMOLOG 1 (MSH1), a plant-specific nuclear gene product that functions in maintaining genome stability in both mitochondria and plastids, on the expression and transmission of phenotypic variability. MSH1 is associated with low-frequency DNA rearrangements mediated by recombination, altered redox properties of the cell, and variegation of the plant. Disruption of MSH1 also gives rise to cytoplasmic male sterility. In the case of cytoplasmic male sterility and variegation, the altered phenotype appears to derive from organellar genomic rearrangement. In this study, the authors report that RNA interference suppression of MSH1 elicits pronounced changes in plant growth patterns for six different plant species. The altered phenotypes include dwarfed growth, reduced internode elongation, enhanced branching, reduced stomatal density, altered leaf morphology, delayed flowering, and extended juvenility, with conversion to perennial growth pattern in short days. Remarkably, these developmental changes, once effected, are stable, heritable, and independent of the RNA interference transgene in subsequent generations, suggesting that these organellar signals influence epigenetic properties of the plant. These results suggest that suppression of MSH1, which occurs under several forms of abiotic stress, triggers a plastidial response process that involves nongenetic inheritance. Abiotic stresses, such as drought, have long been known to inhibit plant growth and thereby decrease crop productivity. Organ growth is driven by both cell proliferation and cell expansion. In the case of Arabidopsis, leaf growth occurs sequentially in time. Initially, all cells in the leaf primordium are dividing, but later in development, cell division ceases from the tip to the base of the leaf, resulting in a cell cycle arrest front moving across the leaf. When plants are confronted with limited water availability, both cell proliferation and cell expansion are affected, leading to smaller leaves composed of fewer and smaller cells. If the stress persists, cells start the transition to cell expansion by exiting the mitotic cell cycle in favor of endoreduplication, during which the genome is replicated, but mitosis does not occur, leading to cells with higher ploidy levels. Claeys et al. (pp. 739–747) now show that this process is dependent on GA signaling. Osmotic stress apparently induces changes in GA metabolism, resulting in stabilization of DELLA proteins, which are responsible for mitotic exit and earlier onset of endoreduplication (DELLA proteins are transcriptional regulators that inhibit GA responses in the absence of GA and are believed to be involved in all GA responses). The earlier onset of endoreduplication induced by osmotic stress is absent in mutants with altered GA levels or DELLA activity. These results coincide with increasing evidence that also implicates DELLAs in regulating the transition to endoreduplication in plant cells.