Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P

https://doi.org/10.1016/j.envexpbot.2015.09.011Get rights and content

Highlights

  • A model based on JIP-test was established to evaluate heat tolerance in croftonweed.

  • Inhibition of the OEC and PSII reaction centers are the initial cause of heat damage.

  • Heat stress destroyed the connectivity of PSII units and stimulated PSI activity.

  • Maintenance of high photosynthetic activity is important for plant heat tolerance.

  • Acquired heat tolerance in croftonweed is due to prior high temperature adaptation.

Abstract

Croftonweed originated from Mexico is a worldwide notorious invasive weed. The objectives of this study were to screen heat tolerance in different croftonweed populations, determine the effect of heat stress on two photosystems and probe the mechanism of acquired heat tolerance. According to conventional tests of plant injury and fast chlorophyll fluorescence rise kinetics, four different croftonweed populations collected from South China were successfully classified into three categories by exposing whole plants to heat treatment at 40 °C: sensitive, intermediate, tolerant. Evidence from the JIP-test indicated that inhibition of the oxygen evolution complexes (OEC) and inactivation of PSII reaction centers (RCs) were the primary cause of heat damage. In mild heat stress (<40 °C), slightly damaged the OEC without creating a visible K-step in the fluorescence rise OJIP curve. In moderate heat stress or stronger (≥40 °C), a pronounced K-step due to irreversible severe damage on the OEC occurred. Additionally, inactivation of PSII RCs, down-regulation of energetic connectivity of PSII units, destruction of PSII antenna architecture, losing overall photosynthetic activity of PSII, increase of PSI activity also took place. Furthermore, the tolerant population had lesser damage degree on photosynthetic capacity relative to intermediate and sensitive populations. Finally, a reliable model, based on the most sensitive parameter PIABS and VK as a characteristic parameter for heat stress, is presented for ranking and identifying heat tolerance in different croftonweed populations. The heat sensitivity index (HSI) is also introduced as an indicator of plant heat sensitivity. The smaller the HSI value is, the higher the level of tolerance to heat stress is. We also found that the tolerance degree of four croftonweed populations to heat stress is significantly correlated to the extreme high temperature. This indicates that acquired heat tolerance in croftonweed populations results from plant adaptation to ambient high temperatures. Acquirement of heat tolerance confers a possible risk for croftonweed to spread further to currently hotter areas.

Introduction

Ageratina adenophora (Spreng.) King & H. Rob. (croftonweed), originated from Mexico, is an alien invasive weed in more than 30 countries and regions worldwide (Xie et al., 2001). It is mainly distributed in the tropical and subtropical areas at latitudes between 37 degrees north and 35 degrees south, with annual average temperatures of 10–22 °C. In the 1940 s, croftonweed was introduced into Yunnan China via Myanmar, and then diffused to Guangxi, Guizhou and Sichuan and Chongqing in southwest China, currently spreading further northward and southward. Its invasion has caused serious local ecosystem destruction and economic loss (Wan et al., 2010, Yu et al., 2014). Temperature and humidity are two major ecological limiting factors that impact croftonweed spread and colonization. Building an expeditious method for screening heat/chilling tolerant plants among different croftonweed populations and probing their tolerance mechanism would allow the identification of those populations most likely to colonize hotter or colder areas. It would be a helpful tool in the risk assessment of croftonweed further spread in China.

In the last two decades, in vivo fast chlorophyll a fluorescence rise kinetics OJIP and JIP-test analysis, based on the so-called “Theory of Energy Fluxes in Biomembranes”, has been widely and successfully used as a powerful tool in the investigation of plant stress physiological states due to its nondestructive, precise and quick characteristic (Strasser et al., 1995, Strasser et al., 2004). The fluorescence rise kinetics OJIP is extremely sensitive to different environmental changes, such as light stress (Krüger et al., 1997, Lazár, 2003, Kalaji et al., 2012), chemical influences (Srivastava et al., 1995, Srivastava et al., 1998, Schansker et al., 2005, Tóth et al., 2005a, Chen et al., 2007, Chen et al., 2011, Xiang et al., 2013), heat (Strasser, 1997, Srivastava et al., 1997, Lu and Zhang, 1999, Tóth et al., 2005b, Tóth et al., 2007, Mathur et al., 2011), chilling or cold (van Heerden et al., 2003, Strauss et al., 2006, Strauss et al., 2007, Gururani et al., 2015), drought (Oukarroum et al., 2007, Oukarroum et al., 2009, Strasser et al., 2010, Goltsev et al., 2012), heavy metal or salt stress (Ouzounidou et al., 1997, Susplugas et al., 2000, Appenroth et al., 2001, Misra et al., 2001, Rivera-Becerril et al., 2002, Xia et al., 2004, Demetriou et al., 2007, Roccotiello et al., 2010, Li and Zhang, 2015), malnutrition (Hermans et al., 2004, Ceppi et al., 2012, Yadavalli et al., 2012, Kalaji et al., 2014), atmospheric CO2 or ozone elevation (Meinander et al., 1996, Clark et al., 2000, Nussbaum et al., 2001, Bussotti et al., 2007, Pollastrini et al., 2014, Sekhar et al., 2014), and disease (Tsimilli-Michael et al., 2000, Christen et al., 2007). Plants exhibit a specific fluorescence rise OJIP curve shape with different peaks after each different stress-treatment (Strasser et al., 2004). A typical fast chlorophyll fluorescence rise kinetics shows a sequence of phases from the initial (FO) to the maximal (FM) fluorescence value, which have been labeled step O (20 μs, all RCs open), J (∼2 ms), I (∼30 ms), and P (equal to FM when all RCs are closed) (Strasser and Strasser 1995). Besides the basic O-J-I-P steps, others also appear in certain conditions, such as the L-step (reflecting the energetic connectivity of the PSII units), the K-step (relating to the inactivation of the oxygen-evolving complex, OEC), or the H- and G-steps in corals and foraminifers (Tsimilli-Michael et al., 1999, Strasser et al., 2004). For example, an additional rapid step, denoted as K-step, appears at about 200 to 300 μs if the samples suffer heat or drought stress. Nitrogen deficiency was also found to result in the appearance of the K-step, the H- and G-steps (Strasser et al., 2004). On the other hand, one to two of the basic O-J-I-P steps will disappear in some stress situations. In PSII-herbicide (e.g., diuron, tenuazonic acid) treated samples, the J-step increases quickly equal to the P level and the IP phase disappears, which contributes to the large accumulation of QA (primary plastoquinone acceptor) in PSII RCs due to the blocking of the electron transport from QA to QB (secondary plastoquinone acceptor) by herbicides (Strasser et al., 2004, Tóth et al., 2005a, Chen et al., 2007). Under strong heat stress (above 44 °C), the J- and I-steps disappear with a concomitant appearance of the K peak as a predominant step in fluorescence rise kinetics because the OEC has been damaged completely (Strasser et al., 2004).

The shape change of the fluorescence rise kinetics OJIP under different environmental cases is highly dependent on the physiological conditions. A quantitative analysis of the OJIP transient has been developed, named as “JIP-test”. The JIP-test translates the shape changes of the OJIP transient to quantitative changes of a constellation of structural, conformational and functional parameters quantifying the behavior of the photosynthetic organisms (for review, see Strasser et al., 2004; reviewed under a fully different nomenclature by Stirbet and Govindjee, 2011). Hence, the JIP-test provides a good access to in vivo vitality screenings, used e.g., to analyze environmental effect on the photosynthetic physiological process, or to screen aimed materials (Strasser et al., 2000, Strasser et al., 2004).

The present study was performed to establish a standard routine to evaluate heat tolerance in different croftonweed populations using fast chlorophyll fluorescence rise kinentics technique. Chlorophyll fluorescence rise kinetics and JIP-test parameters are frequently used to assess plant physiological responses to heat stress. However, an easy systemic analysis method on JIP-test for high-throughput screening for heat tolerance in plants has never been built. Thus, we aimed to test two hypotheses as following.

Firstly, PIABS and the heat sensitivity index (HSI), a parameter calculated from PIABS and VK, would be sensitive enough to evaluate the response of differrent croftonweed populations to heat stress and to rank them according to heat stress tolerance degree.

Secondly, the high photosynthesis, especially high activity of the OEC and PSII RCs, maintained after heat stress is necessary to heat tolerance in croftonweed populations.

Here, we determined chlorophyll fluorescence rise kinetics OJIP of heat-treated whole plants of four croftonweed populations and checked the capacity of this technique for screening heat tolerance. A further analysis was carried out to identify, localise and quantify effects of heat stress on two photosystems, and investigate the correlation between the effects on photosynthetic process and the level of heat stress. Finally, a model was developed for evaluating plant heat tolerance based on two characteristic JIP-test parameters for heat stress. In this model, the absolute value of the slope (K) of the linear relationship between fluorescence parameters logPIABS and VK is confirmed as an indicator of heat tolerance level. We also found that heat tolerance of different croftonweed populations was developed due to the heat adaptation to local climate conditions.

Section snippets

Sample collection and plant culture

Croftonweed seeds were collected in 2003–2004 at four locations (Latitude N/ Longitude E) in two provinces in South China: Dali city (DL, 25°33′/100°14′), Chuxiong city (CX, 25°02′/101°31′), Yuanjiang city (YJ, 23°36′/101°59′) of Yunnan province and Huangguoshu city (HGS, 25°58′/105°39′) of Guizhou province (Fig. 1A). Seeds from the four geographically distinct populations were planted in plastic cups containing a mixture of peat, vermiculite and perlite (3:1: 0.5). Seedlings were grown under

Identification of heat tolerance of four croftonweed populations

The four croftonweed populations (Fig. 1A) could be grouped into heat tolerant, intermediate and sensitive based on the whole-plant damage level after being exposed to 40 °C for 72 h (Fig. 1B). DL plants exhibited highly sensitive to heat treatment because whole plants already died totally. Conversely, YJ plants only developed slight damage on some leaves and are therefore considered tolerant to heat stress. HGS and CX were intermediately tolerant to heat for some leaves keeping alive. To further

High temperature affects on PSII and PSI

High temperature affects a broad spectrum of cellular components and metabolic processes (Sung et al., 2003). Photosynthesis is among the most sensitive physiological processes to high temperature stress, and maintenance of high photosynthetic activity is important for plant tolerance to heat stress (Liu and Huang, 2008). Extensive studies demonstrate that heat treatment can cause inactivation of OEC, inhibition of electron transport, and decrease in PSII photochemical efficiency (De Ronde et

Acknowledgements

This work was supported by the Fundamental Research Funds for the Central Universities (KYZ201530), NSFC (31572066, 31272080), Special Funds of the State Environmental Protection Industry (201409061) and Jiangsu Science & Technology Pillar Program (BE20014397). The authors thank Bernal E. Valverde (Investigación y Desarrollo en Agricultura Tropical, Costa Rica) for helpful comments and improving the manuscript.

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