Lilin Zhao

Asymmetric sensitivity of first flowering date to warming and cooling in alpine plants

Understanding how flowering phenology responds to warming and cooling (i.e., symmetric or asymmetric response) is needed to predict the response of flowering phenology to future climate change that will happen with the occurrence of warm and cold years superimposed upon a long-term trend. A three-year reciprocal translocation experiment was performed along an elevation gradient from 3200 m to 3800 m in the Tibetan Plateau for six alpine plants. Transplanting to lower elevation (warming) advanced the first flowering date (FFD) and transplanting to higher elevation (cooling) had the opposite effect. The FFD of early spring flowering plants (ESF) was four times less sensitive to warming than to cooling (by −2.1 d/°C and 8.4 d/°C, respectively), while midsummer flowering plants (MSF) were about twice as sensitive to warming than to cooling (−8.0 d/°C and 4.9 d/°C, respectively). Compared with pooled warming and cooling data, warming alone significantly underpredicted 3.1 d/°C for ESF and overestimated 1.7 d/°...

Chemical Signals Synchronize the Life Cycles of a Plant-Parasitic Nematode and Its Vector Beetle

The pinewood nematode Bursaphelenchus xylophilus has caused severe damage to pine forests in large parts of the world [1-4]. Dispersal of this plant-parasitic nematode occurs when the nematode develops into the dispersal fourth larval stage (LIV) upon encountering its insect vector, the Monochamus pine sawyer beetle, inside an infected pine tree [5-9]. Here, we show that LIV formation in B. xylophilus is induced by C16 and C18 fatty acid ethyl esters (FAEEs), which are produced abundantly on the body surface of the vector beetle specifically during the late development pupal, emerging adult, and newly eclosed adult stages. The LIV can then enter the tracheal system of the adult beetle for dispersal to a new pine tree. Treatment of B. xylophilus with long-chain FAEEs, or the PI3 kinase inhibitor LY294002, promotes LIV formation, while Δ7-dafachronic acid blocks the effects of these chemicals, suggesting a conserved role for the insulin/IGF-1 and DAF-12 pathways in LIV formation. Our work provides a mechanism by which LIV formation in B. xylophilus is specifically coordinated with the life cycle of its vector beetle. Knowledge of the chemical signals that control the LIV developmental decision could be used to interfere with the dispersal of this plant-parasitic nematode.

The Ratio and Concentration of Two Monoterpenes Mediate Fecundity of the Pinewood Nematode and Growth of Its Associated Fungi

The pinewood nematode (PWN) Bursaphelenchus xylophilus, vectored primarily by the sawyer beetle, Monochamus alternatus, is an important invasive pest and causal agent of pine wilt disease of Chinese Masson pine, Pinus massoniana. Previous work demonstrated that the ratios and concentrations of α-pinene∶β-pinene differed between healthy trees and those trees containing blue-stain fungus (and M. alternatus pupae). However, the potential influence of the altered monoterpene ratios and concentrations on PWN and associated fungi remained unknown. Our current results show that low concentrations of the monoterpenes within petri dishes reduced PWN propagation, whereas the highest concentration of the monoterpenes increased PWN propagation. The propagation rate of PWN treated with the monoterpene ratio representative of blue-stain infected pine (α-pinene∶β-pinene = 1∶0.8, 137.6 mg/ml) was significantly higher than that (α-pinene∶β-pinene = 1∶0.1, 137.6 mg/ml) representative of healthy pines or those damaged by M. alternatus feeding, but without blue stain. Furthermore, inhibition of mycelial growth of associated fungi increased with the concentration of the monoterpenes α-pinene and β-pinene. Additionally, higher levels of β-pinene (α-pinene∶β-pinene = 1∶0.8) resulted in greater inhibition of the growth of the associated fungi Sporothrix sp.2 and Ophiostoma ips strains, but had no significant effects on the growth of Sporothrix sp.1, which is the best food resource for PWN. These results suggest that host monoterpenes generally reduce the reproduction of PWN. However, PWN utilizes high monoterpene concentrations and native blue-stain fungus Sporothrix sp.1 to improve its own propagation and overcome host resistance, which may provide clues to understanding the ecological mechanisms of PWNs successful invasion.

A native fungal symbiont facilitates the prevalence and development of an invasive pathogen-native vector symbiosis

Invasive pathogen-insect symbioses have been extensively studied in many different ecological niches. Whether the damage of symbioses in different introduced regions might be influenced by other microorganisms has, however, received little attention. Eight years of field data showed that the varied levels of the nematode and beetle populations and infested trees of the invasive Bursaphelenchus xylophilus--Monochamus alternatus symbiosis were correlated with patterns in the isolation frequencies of ophiostomatoid fungi at six sites, while the laboratory experiments showed that the nematode produced greater numbers of offspring with a female-biased sex ratio and developed faster in the presence of one native symbiotic ophiostomatoid fungus, Sporothrix sp. 1. Diacetone alcohol (DAA) from xylem inoculated with Sporothrix sp. 1 induced B. xylophilus to produce greater numbers of offspring. Its presence also significantly increased the growth and survival rate of M. alternatus, and possibly explains the prevalence of the nematode-vector symbiosis when Sporothrix sp. 1 was dominant in the fungal communities. Studying the means by which multispecies interactions contributed to biogeographical dynamics allowed us to better understand the varied levels of damage caused by biological invasion across the invaded range.

Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle

Insect vectors are required for the transmission of many species of parasitic nematodes, but the mechanisms by which the vectors and nematodes coordinate their life cycles are poorly understood. Here, we report that ascarosides, an evolutionarily conserved family of nematode pheromones, are produced not only by a plant-parasitic nematode, but also by its vector beetle. The pinewood nematode and its vector beetle cause pine wilt disease, which threatens forest ecosystems world-wide. Ascarosides secreted by the dispersal third-stage nematode LIII larvae promote beetle pupation by inducing ecdysone production in the beetle and up-regulating ecdysone-dependent gene expression. Once the beetle develops into the adult stage, it secretes ascarosides that attract the dispersal fourth-stage nematode LIV larvae, potentially facilitating their movement into the beetle trachea for transport to the next pine tree. These results demonstrate that ascarosides play a key role in the survival and spread of pine wilt disease.

Phenotypic plasticity of reproductive traits in response to food availability in invasive and native species of nematode

Invasive species cause severe ecological and economic damage; however, the mechanisms underlying their successful invasion often remain elusive. In the case of Bursaphelenchus xylophilus, a global quarantine pest which invaded Asia and Europe, it has been suggested that this species possesses highly competitive abilities, which promotes its establishment and rapid spread. To explore biological traits that may explain its highly competitive abilities, we focused on expression of phenotypic plasticity in response to the food conditions experienced by the females during their development as juveniles in the invasive species B. xylophilus and native species Bursaphelenchus mucronatus. We report an unexpected significant difference of phenotypic trade-off between egg number and egg size in the invasive species B. xylophilus and native species B. mucronatus. This leads to superior propagation ability of invasive species, under high and low food conditions in culture. These effects reflect adaptive optimal resource allocation where more eggs are produced in favorable environments to enhance population viability. Furthermore, we show that B. xylophilus eggs hatched earlier than B. mucronatus when their parents experienced high food availability. Thus, this study revealed, for the first time, phenotypic plasticity of reproductive traits in B. xylophilus which empowers the species a competitive advantage relative to their native counterpart B. mucronatus when they are under different range of food availability. These results are a step towards answering the vital question of how an exotic invasive species exclude a native species from its original niche.

Seasonal and interannual variations of ecosystem photosynthetic features in an alpine dwarf shrubland on the Qinghai-Tibetan Plateau, China

Ecosystem photosynthetic characteristics are of utmost importance for the estimation of regional carbon budget, but such characteristics are not well understood in alpine regions. We collected CO2 flux data measured by eddy covariance technique over an alpine dwarf shrubland on the Qinghai-Tibetan Plateau during years 2003–2010; and we quantified the temporal patterns of ecosystem apparent quantum yield (a), saturated photosynthetic rate (Pmax), and ecosystem dark respiration (RDe). Results showed that the strong seasonality of a and RDe was driven mainly by air temperature (Ta), whereas that of Pmax was much more determined by leaf area index rather than abiotic factors. Diurnal thermal fluctuation inhibited significantly the daytime photosynthetic capacity. Stepwise regression revealed that the seasonal deviations of a, Pmax, and RDe were significantly controlled by Ta. The annual a was regulated mainly by annual growing season Ta, which indicated that the response of ecosystem a was instant. The annual variations of Pmax correlated positively with soil temperature 5 cm below ground (Ts) of the annual nongrowing season and those of RDe related negatively with the annual nongrowing season precipitation. We suggested that a lagged response regulated the annual Pmax and the annual RDe. Annual deviations of a and RDe were both significantly controlled by annual Ts, and those of Pmax were marginally determined by annual PPFD. Thus, the future warming scenario, especially significant for nongrowing seasonal warming in the Qinghai-Tibetan Plateau, would favor ecosystem photosynthetic capacity in the alpine dwarf shrubland.

Ascarosides Promote the Prevalence of Ophiostomatoid Fungi and an Invasive Pathogenic Nematode, Bursaphelenchus xylophilus

Understanding the coevolution of pathogens and their associated mycoflora depend upon a proper elucidation of the basis of their chemical communication. In the case of pine wilt disease, the mutual interactions between cerambycid beetles, invasive pathogenic nematodes, (Bursaphelenchus xylophilus) and their symbiotic ophiostomatoid fungi provide a unique opportunity to understand the role of small molecules in mediating their chemical communication. Nematodes produce ascarosides, a highly conserved family of small molecules that serve essential functions in nematode biology and ecology. Here we demonstrated that the associated fungi, one of the key natural food resources of pine wood nematodes, can detect and respond to these ascarosides. We found that ascarosides significantly increase the growth of L. pini-densiflorae and Sporothrix sp. 1, which are native fungal species in China that form a symbiotic relationship with pinewood nematodes. Hyphal mass of L. pini-densiflorae increased when treated with asc-C5 compared to other ophiostomatoid species. Field results demonstrated that in forests where higher numbers of PWN were isolated from beetle galleries, L. pini-densiflorae had been prevalent; the same results were confirmed in laboratory studies. Furthermore, when treated with asc-C5, L. pini-densiflorae responded by increasing its production of spores, which leads to a higher likelihood of dispersal by insect vectors, hence explaining the dominance of L. pini-densiflorae over S. sp. 1 in the Tianwang and Nanlu Mountains within the Northern Forestry Centre of China. These findings provide an emphatic representation of coevolution of pine wood nematode and its associated fungi. Our results lay a broader foundation for a better understanding of inter-kingdom mutualisms and the chemical signals that mediate their establishment.