*Article* **Adaptability Mechanisms of Japonica Rice Based on the Comparative Temperature Conditions of Harbin and Qiqihar, Heilongjiang Province of Northeast China**

**Muhammad Shahbaz Farooq 1, Amatus Gyilbag 1, Ahmad Latif Virk <sup>2</sup> and Yinlong Xu 1,\***

<sup>1</sup> Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing 100081, China; mshahbazfarooq786@gmail.com (M.S.F.); amatusmike@yahoo.com (A.G.)

**\*** Correspondence: xuyinlong@caas.cn

**Abstract:** Japonica rice has been considerably impacted from climate change, mainly regarding temperature variations. Adjusting the crop management practices based on the assessment of adaptability mechanisms to take full advantage of climate resources during the growing season is an important technique for japonica rice adaptation to climate changed conditions. Research based on the adaptability mechanisms of japonica rice to temperature and other environmental variables has theoretical and practical significance to constitute a theoretical foundation for sustainable japonica rice production system. A contrived study was arranged with method of replacing time with space having four different japonica cultivars namely Longdao-18, Longdao-21, Longjing-21, and Suijing-18, and carried out in Harbin and Qiqihar during the years 2017–2019 to confer with the adaptability mechanisms in terms of growth, yield and quality. The formation of the grain-filling material for superior and inferior grains was mainly in the middle phase which shared nearly 60% of whole grain-filling process. Maximum yield was noticed in Longdao-18 at Harbin and Qiqihar which was 9500 and 13,250 kg/ha, respectively. The yield contributing components fertile tillers, number of grains per panicle, and 1000-grain weight were higher at Qiqihar; therefore, there was more potential to get higher yield. The data for grain-filling components demonstrated that the filling intensity and duration at Qiqihar was contributive to increase the grain yield, whereas the limiting agents to limit yield at Harbin were the dry weights of inferior grains. The varietal differences in duration and time of day of anthesis were small. Across all cultivars and both study sites, nearly 85% of the variation of the maximum time of anthesis could be justified with mean atmospheric temperature especially mean minimum temperature. Mean onset of anthesis was earliest in Longdao-21 at Harbin, whereas it was latest in Longdao-18 at Qiqihar. The maximum time to end anthesis and the longest duration of anthesis were taken by Longdao-18, i.e., 9.0 hasr and 4.2 h, respectively. Chalkiness and brown rice percentages were elevated at Qiqihar showing Harbin produced good quality rice. This study investigated the adaptability mechanisms of japonica rice under varying temperature conditions to distinguish the stress tolerance features for future sustainability and profitability in NEC. It was concluded that there is an adaptive value for anthesis especially regarding Tmin and, moreover, earlier transplantation may produce tall plants. The results demonstrated that high temperature at the onset of anthesis at the start of the day enhanced the escape from high temperature later during the day. Early transplantation is recommended in NEC because earlier anthesis during humid days rendered for potential escape from high ambient temperature later during that day. Temperature influenced japonica rice significantly and coherently, whereas the influence of growing season precipitation was not significant. Daily mean sunshine influenced the japonica rice significantly, but the impact was less spatially coherent. The results foregrounded the response of the japonica rice to external driving factors focusing climate, but ignored socioeconomic suggesting emphasis on both driving factors to target future research and render important insights into how japonica rice can adapt in mid-high-latitude regions.

**Citation:** Shahbaz Farooq, M.; Gyilbag, A.; Virk, A.L.; Xu, Y. Adaptability Mechanisms of Japonica Rice Based on the Comparative Temperature Conditions of Harbin and Qiqihar, Heilongjiang Province of Northeast China. *Agronomy* **2021**, *12*, 2367. https://doi.org/10.3390/ agronomy11112367

Academic Editor: Arnd Jürgen Kuhn

Received: 6 October 2021 Accepted: 16 November 2021 Published: 22 November 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

<sup>2</sup> College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China; virk3813b64@yahoo.com

**Keywords:** japonica rice; adaptability mechanisms; grain-filling; anthesis; grain yield; Northeast China

#### **1. Introduction**

Global mean surface temperatures are expected to be higher from the present by 1–3 ◦C at the end of year 2100 [1]. China's climate has become drier and warmer compared to the 20th century [2]. Northeast China (NEC), one of the major rice producing regions in China, experienced the most obvious warming since last century [3], but the most evident warming has been observed since the 1980s with an annual mean temperature rise of 1.0–2.5 ◦C. In NEC, reduction in precipitation was seen during summer as the mean rainfall has been decreasing since 1965 [3], whereas increase in temperature has been observed in winter [4]. In NEC, the temperature was higher during 1920–1930, after three decades, it started to decrease, and thereafter again during the 1970s–1980s, it started to become higher [5]. For NEC, the average rise in daily minimum temperature was more obvious than the daily maximum temperature which noticeably narrowed the diurnal temperature range [6]. There is vulnerability to semi-arid areas in NEC because of periodic drought stress as most of the lakes are even disappearing because of declining precipitation and ground water levels.

Production of cereals and majorly rice is one of the major characteristics of food security and grown in over 100 countries around the globe, fulfilling the dietary requirements of millions of people, and considered as an extremely thermosensitive cereal [7,8]. Heat stress events are expected to become frequent, and intensely impact crop growth and grain yield [9–11]. In recent decades, the global temperature has increased due to activities of continuously increasing global population such as deforestation, spread of industrial setups, and enhanced emissions of greenhouse gases (GHGs) [12,13]. Extreme climatic events are adverse for crop growth and development, such as heat stress produce impacts on net yield [14]. High temperature stress on reproductive growth stage rice has become a global issue. Therefore, researching the mechanisms of impacts of climatic variability during different rice growth stages and tolerance against this variability to minimize the losses have become interest among global scientists.

Cereals share 27% of total cultivable area in China where rice is the major crop, sharing 35% of the total food demand nationwide [10,15]. NEC harvests 20% of the China's marketable food grain where rice shares highest quantity [16,17]. Rice is considered as a highly climate-sensitive cereal, and NEC has been observed as one of the most susceptible regions to climate change [10]. Several studies have shown an increase in mean surface temperature with an average warming trend of 0.38–0.65 ◦C per decade during last five decades [18] which favored the cultivation of seasonal flooded rice. Seasonally grown flooded rice in NEC has brought significant changes in recent decades as it is a major source of methane emissions [19], as over 10% of global methane emissions are being released in the atmosphere due to rice cultivation [20]. Consequently, the dynamic changes in the rice statistics and relationship with climatic variabilities in NEC along with other causes of GHGs emissions are of great importance for eco-efficient japonica rice sustainability [21,22].

In NEC particularly in Heilongjiang Province, rice cultivation has been motivated among local communities by many features such as balance in market prices and climatic variabilities [23–25]. Over the last three decades (1980–2010), rice production in Heilongjiang Province has been increased from 3 to 13% of total national rice production, mostly owing to the speedy growth of rice cultivating areas in NEC [15]. Many studies have done the investigations on variation of rice production due to the impacts of climatic variabilities in NEC—though up till now the outcomes are still confusing with none of the sound adjustive measures—by assessing the adaptability mechanisms regionally [26–28]. Ref. [27] revealed that net grain yield is reduced due to the effect of climate warming, but research conducted in South China and NEC unveiled a boost in rice grain yield at high-latitude regions [26,28].

Rice grain yield is comprised of two major fundamentals: rice yield and planting area [29]. Previous studies uncovered that a nearly 92% increase (about 4.23 mha) in single rice cropping regions in China has occurred in NEC between 1949 and 2013 [23]. Only native yield analyses cannot reflect the natural resource management and food security issues behind higher production of rice perfectly [15,21,30]. Moreover, the primary association among climate variability with japonica rice growth and development, adaptability mechanisms of japonica rice, and production have received fewer attention in high latitudes of China.

The japonica rice growth has been severely affected due to high temperature above the normal range in areas where the temperature has surpassed the optimum range (28/22 ◦C). It has been reported that rice yield decreased by 7–8% with an increase of each 1 ◦C temperature at the maximum daytime/minimum night time from 28/21 to 34/27 ◦C, respectively [31,32]. Moreover, rice production was greatly impacted due to variation in internal climate with an increase in the interannual climate predicted to be highly variable under frequent temperature stress events during the reproductive growth stages [33]. Therefore, this prediction rejects the hypothesis of expected benefits of estimated rise in atmospheric CO2 on rice plant growth [34].

Among all critical growth stages, booting and flowering are comparatively more sensitive to temperature stresses [35,36]. During early stages of booting, the plant is occupied with low panicles, often at or below flood water level, and is safer due to plant tissues. However, cells undergoing the meiosis have been noticed with damages of cold temperature stress [37,38] during microspore release from tetrads [39]. Sensitive stage of booting starts approximately 7 and 15 d between panicles' initiation and the end of panicle initiation, respectively [40,41]. The upper part of the plant and the spikelets exposed and emerged during the flowering phase are more vulnerable to temperature stress [38,42], which may cause failure or damage of the pollens [38,43,44]. Climatic variability greatly affects the grain yield due to impacts on grain-filling. There are several explanations for poor grain-filling and low grain weight of the superior and inferior spikelets such as low enzyme activity in the conversion of sucrose to starch [11,45–47], hormonal imbalance [11,45], and assimilating transportation barriers [46,48]. It has been revealed that at the early grain-filling stage, the concentrations of soluble carbohydrates in the inferior spikelets are higher than those in the superior spikelets, suggesting that assimilating the supply is not the main reason for poor spikelet grain-filling among inferior grains [47].

Warming stress at flowering and grain-filling stages can reduce the net grain yield through spikelet sterility and shortening the duration of the grain-filling phase [49,50]. The growing degree days (GDD) for a specific cultivar for flowering are almost the same when grown under varying temperature conditions within the temperature ranges of optimum and base temperatures. Growth of superior and inferior grains was faster at higher temperatures but with a reduced grain-filling period [51]. There is an inverse correlation of the length of daily average temperature with the ripening period; therefore, the temperature below or above the optimum range will reduce the grain-filling period. Poor grain-filling decreases the grain weight as a result of rice plant exposure to frequent and continuous high temperature stress during the grain-filling stage [50]. Meanwhile, higher temperature stress during the grain-filling stage enhances the demand for more assimilations avoiding the production of chalky grains [52]. Higher temperature also impacts the developmental and cellular processes leading towards poor grain quality [53,54]. Drought prevalence during grain-filling adversely impacts the grain weight of superior and inferior grains and also reduces the grain quality [55]. Considering the declining water resources in NEC, the future research studies must be focusing on a genotype selection tool in future breeding varietal development programs for screening of drought tolerant japonica rice

cultivars with considerations of the adaptability mechanisms of specific cultivars during the grain-filling period for efficient grain-filling duration and rate.

The research gap in NEC is calling the researchers' focus to address climate change impacts on japonica rice growth and yield, thereby suggesting the possible concrete adjustive measures for sustainable japonica rice production systems in NEC. Climatic variabilities have already been exacerbated under climate change, e.g., temperature stress including high and low, humidity, drought, soil salinity, and submergence [8]. Higher temperature stress can greatly damage rice yield by two principles: firstly, high maximum temperature stress combined with higher humidity causing spikelet sterility and reduced quality of grains [54]. Secondly, through higher night-time temperature stress which usually reduces the process of assimilates accumulation. Thus, if response mechanisms could have been investigated at regional and local scales of NEC, then it could possibly help in development of improved rice germplasm with better resistance against specific climatic stress.

Past research in NEC has not focused on the japonica rice adaptation to climate change in NEC. Limited literature is available to apprehend the adaptability mechanisms of the japonica rice cultivars under varying temperature conditions of NEC. Majorly, previous studies have ignored to comprehend the transitions in eco-physiology of japonica rice cultivars to temperature variations. Furthermore, a lack in understanding of the self-adaptability of japonica rice for its necessary threatened the adaptation which was possible with suitable outside interventions. A lack of evaluation of adaptability mechanisms and thereby possible adjustive measures reduced the adaptation process of japonica rice in NEC. To evaluate the sound possible adjustive measures against environmental variabilities in NEC, it is necessary to analyze the adaptability mechanisms of japonica rice cultivars to different temperature conditions. Comparative assessment of japonica rice adaptability mechanisms under climatic variations at regional and local scales of NEC is necessary to overcome the main research gap of past studies. Rice originally is a semiaquatic phylogenetic plant with unique features of susceptibility and self-adaptability against climatic variability [56] which help to possibly adjust the rice production system. Therefore, there are considerable risks to japonica rice system sustainability branching from climatic variability, but addressing the adaptability mechanisms at local scales in NEC and then delivering necessary adjustive strategies can produce a sustainable and wide range of japonica rice production system under varying climatic conditions to encourage the regional sustainability of japonica rice in NEC [57]. Therefore, this study hypothesized that deep investigations of adaptability mechanisms among short- and long-duration japonica rice cultivars under varying temperature conditions pave the way for better adaptation with possible adjustive measures in management practices. To have concrete estimations of the adaptability mechanisms of japonica rice to different temperature changed conditions, this study was designed with the following objectives: (1) providing deep insights into the adaptability mechanisms of japonica rice to climatic driving factors at different growth phases; (2) identifying and evaluating possible potential adjustive measures in management practices to adapt and sustain japonica rice production.
