Toward Designing Tulips for a Warmer World
Most cultivated tulips (Tulipa gesneriana) are produced in The Netherlands, which has a temperate climate resembling the Central Asian climate in which they originated. The growth cycle of cultivated tulips starts in autumn, when the bulbs are planted in the field. At that time, all organs, including the flower, are already present inside the bulb. A subsequent period of prolonged cold is required for rapid stem elongation as well as for internal preparation of the flower to bloom in spring. After this cold winter period, the stem elongates, the leaves stretch and unfold, and blooming occurs in April or May. The mother bulb is completely consumed after blooming, and the main daughter bulb replaces the mother bulb. Increasing temperatures in the spring are assumed to induce the vegetative-to-reproductive phase change (floral induction) at the shoot apical meristem in the daughter bulb, leading to the development of the floral organs and the induction of dormancy. Once the flower is completely developed inside the bulb, the life cycle starts anew. In The Netherlands, the warm winters and high temperatures during spring in recent years interfered with the floral induction process and induced an early transition from vegetative to reproductive development, resulting in dehydration of the flower (floral bud blasting) or low-quality tulip flowers. This problem calls for the development of new cultivars that are adapted to this climate change; hence, detailed molecular knowledge of the process is required. To shed light on the gene network that controls flowering in tulip, Leeggangers et al. (pp. 1904–1919) undertook a genome-wide approach to elucidate the molecular mechanism underlying the floral induction and the integration of temperature responses in tulip. Their results indicate that long before morphological changes occur in the shoot apical meristem, the expression of floral repressors in tulip is suppressed by increased ambient temperatures, leading either directly or indirectly to the activation of potential flowering activators shortly before the commencement of the phase change.
Heteroblastic Development of Transfer Cells: A Role for MicroRNA
Transfer cells (TCs) play critical roles in membrane transport of solutes at various sites within plants and between plants and their environment. This transport capacity is conferred by inward wall protuberances that extend into the cell lumen. These ingrowths function to enhance the area of surrounding plasma membrane, therefore increasing surface-to-volume ratio of the TC and consequently promoting the transmembrane flux of solutes. Across the plant kingdom, the occurrence of TCs is proposed to be an indicator of anatomical locations where intensive transport occurs. In Arabidopsis (Arabidopsis thaliana), phloem parenchyma (PP) cells in the minor vein network of leaves and sepals can develop wall ingrowths to become PP TCs. Wall ingrowths in these PP TCs are typically bulky and predominantly abut sieve elements and to a lesser extent companion cells. PP TCs have been assumed to facilitate the efflux of photoassimilates. Nguyen et al. (pp. 1676–1691) now report that wall ingrowth deposition in PP TCs in leaf veins of Arabidopsis represents a novel trait of heteroblasty. PP TCs with extensive wall ingrowths are ubiquitous in mature cotyledons and juvenile leaves, but dramatically less so in mature adult leaves, an observation consistent with PP TC development reflecting vegetative phase change in Arabidopsis. Consistent with this conclusion, the abundance of PP TCs with extensive wall ingrowths varied across rosette development in three ecotypes displaying differing durations of juvenility. PP TC development across juvenile, transition, and adult leaves correlated positively with levels of miR156, a major regulator of the vegetative phase change in plants.
A Salivary Effector Aids in Brown Planthopper Feeding on Rice Plants
Herbivory-induced plant cell wall modifications play an important role in deterring herbivory. Modified cell walls not only act as physical defenses against herbivores by enhancing the mechanical hardness of plant tissues but also reduce the digestibility of food for herbivores, thereby functioning as the first layer of defense against herbivores. In response, herbivores have evolved the capacity to suppress and circumvent these plant defenses through the release of effectors. Herbivores can secrete salivary plant cell wall-degrading enzymes such as cellulases (consisting of endo-β-1, 4-glucanases and β-glucosidases) and pectinases to degrade plant cell walls.
The brown planthopper Nilaparvata lugens is a major insect pest of rice (Oryza sativa) in Asia. After landing on plants, the brown planthopper feeds by sucking the phloem sap. Ji et al. (pp. 1920–1932) have discovered a salivary endo-β-1,4-glucanase (NlEG1) that is secreted into rice plants by brown planthoppers. Silencing NlEG1 reduces the food intake, mass, survival, and fecundity of brown planthoppers feeding on rice plants. By contrast, NlEG1 silencing had only a small effect on the survival rate of brown planthoppers raised on an artificial diet. Moreover, NlEG1 secreted by brown planthoppers did not elicit the production of the defense-related signal molecules salicylic acid, jasmonic acid, and jasmonoyl-Ile in rice. The authors suggest that NlEG1 enables the brown planthopper’s stylet to reach the phloem by degrading the cell wall defenses induced in rice plants in response to herbivory.
Insights into Calmodulin-Interacting Proteins
Calmodulin (CaM) and closely related CaM-like polypeptides are principal sensors of Ca2+ signals. The plant-specific IQ67 DOMAIN (IQD) family has emerged as possibly the largest class of CaM-interacting proteins with undefined molecular functions and biological roles. Bürstenbinder et al. (pp. 1692–1708) show that the 33 members of the IQD family in Arabidopsis differentially localize to multiple and distinct subcellular sites, including microtubule (MT) arrays, plasma membrane subdomains, and nuclear compartments. Intriguingly, the various IQD-specific localization patterns coincide with the subcellular patterns of IQD-dependent recruitment of CaM, suggesting that the diverse IQD members sequester Ca2+-CaM signaling modules to specific subcellular sites for precise regulation of Ca2+-dependent processes. Because MT localization is a hallmark of most IQD family members, the authors quantitatively analyzed GFP-labeled MT arrays in Nicotiana benthamiana cells transiently expressing GFP-IQD fusions and observed IQD-specific MT patterns, which point to a role of IQDs in MT organization and dynamics. Indeed, misexpression of select IQD proteins in Arabidopsis altered cellular MT orientation, cell shape, and organ morphology. Because IQDs share biochemical properties with scaffold proteins, the authors propose that the IQD family provides an assortment of platform proteins for integrating CaM-dependent Ca2+ signaling at multiple cellular sites to regulate cell function, shape, and growth.
Sites of Water Evaporation from within Leaves
Current available evidence suggests that the location of the sites of evaporation is important for many questions across plant physiology, including patterns of leaf isotopic enrichment, maintenance of mesophyll water status, stomatal regulation, and interpretation of measured stomatal and leaf hydraulic conductances. To resolve these questions, Buckley et al. (pp. 1763–1782) argue that models must extend beyond the substomatal cavity to include realistic depictions of tissues and conditions deeper in the leaf. However, most previous studies of the evaporating sites have been confined to single species or have used generic models that are not suitable for exploring the effects of species variation in leaf internal anatomy. To overcome these limitations, the authors used an anatomically and biophysically explicit model of coupled heat and water transport outside the xylem, MOFLO 2.0, parameterized for 14 diverse angiosperm species, to analyze the sites of evaporation within leaves in relation to anatomy and environmental conditions. Their objectives were to map the distribution of net evaporation across tissues within a single leaf areole, to determine how that distribution is affected by leaf anatomy and environmental conditions and to explore implications of the evaporating sites for measurements and inferences across plant physiology. Their results corroborate earlier predictions that most evaporation occurs from the epidermis at low light and moderate humidity but that the mesophyll contributes substantially when the leaf center is warmed by light absorption and more so under high humidity.
Genome-Wide Analysis of Temperature-Induced Fatty Acid Desaturation
Biogeographic studies suggest that the degree of fatty acid unsaturation in oilseeds has played a major role in adapting plants to temperature. The enzymes that are primarily responsible for producing polyunsaturated fatty acids in seed oils are the microsomal ω-6 and ω-3 fatty acid desaturases FAD2 and FAD3, which act in sequence to convert oleic acid (18:1) to linoleic acid (18:2) and then to α-linolenic acid (18:3), while the fatty acid is esterified to the sn-2 position of phosphatidylcholine. Temperature can influence the degree of microsomal fatty acid desaturation indirectly through its effects on substrate availability. However, there also is evidence that FAD2 and FAD3 are regulated directly by temperature. Whether this regulation occurs at the level of gene expression appears to vary depending upon the species, tissue, and gene in question. Many previous studies have exploited genetic approaches to investigate the function of fatty acid desaturation in plant temperature adaptation. However, no studies appear to have used genetic variation in plants to study the underlying regulatory mechanisms. Menard et al. (pp. 1594–1605) have characterized the response of Arabidopsis seed lipids to variation in ambient temperature and found that warm temperatures inhibit both ω-6 and ω-3 desaturation in phosphatidylcholine. Analyses of 19 parental accessions showed that significant natural variation exists in the temperature responsiveness of ω-6 desaturation. A combination of quantitative trait locus analysis and genome-wide association studies suggests that ω-6 desaturation is largely controlled by cis-acting sequence variants in the FAD2 5′ untranslated region intron that determines the expression level of the gene. However, the temperature responsiveness of ω-6 desaturation is controlled by a separate quantitative trait locus on chromosome 2.