Research Article: Diurnal biomarkers reveal key photosynthetic genes associated with increased oil palm yield

Date Published: March 11, 2019

Publisher: Public Library of Science

Author(s): Bee Keat Neoh, Yick Ching Wong, Huey Fang Teh, Theresa Lee Mei Ng, Soon Huat Tiong, Tony Eng Keong Ooi, Mohd. Zairey Md. Zain, Mohd. Amiron Ersad, Chee Keng Teh, Heng Leng Lee, Siti Khadijah Mohd Rais, See Siang Cheah, Fook Tim Chew, Harikrishna Kulaveerasingam, David Ross Appleton, Anil Kumar Singh.

http://doi.org/10.1371/journal.pone.0213591

Abstract

To investigate limiters of photosynthate assimilation in the carbon-source limited crop, oil palm (Elaeis guineensis Jacq.), we measured differential metabolite, gene expression and the gas exchange in leaves in an open field for palms with distinct mesocarp oil content. We observed higher concentrations of glucose 1-phosphate, glucose 6-phosphate, sucrose 6-phosphate, and sucrose in high-oil content palms with the greatest difference being at 11:00 (p-value ≤0.05) immediately after the period of low morning light intensity. Three important photosynthetic genes were identified using differentially expressed gene analysis (DEGs) and were found to be significantly enriched through Gene Ontology (GO) and pathway enrichment: chlorophyll a-b binding protein (CAB-13), photosystem I (PSI), and Ferredoxin-NADP reductase (FNR), particularly for sampling points at non-peak light (11:00 and 19:00), ranging from 3.3-fold (PSI) and 5.6-fold (FNR) to 10.3-fold (CAB-13). Subsequent gas exchange measurements further supported increased carbon assimilation through higher level of internal CO2 concentration (Ci), stomatal conductance (gs) and transpiration rate (E) in high-oil content palms. The selection for higher expression of key photosynthesis genes together with CO2 assimilation under low light is likely to be important for crop improvement, in particular at full maturity and under high density planting regimes where light competition exists between palms.

Partial Text

Oil palm (Elaeis guineensis) is the world’s most productive oil crop on a per hectare basis and is, therefore, an important source of dietary oils and fats. Although total fruit yield, fruit bunch weight and especially mesocarp oil content are reported to be heritable [1–3], negative correlations do exist for these traits, suggesting a degree of source limitation. Also, there is a significant gap between potential and actual yield in the field caused by factors such as planting density (light competition), pollination efficiency (poor fruit formation), water and nutrient supply, field management practices, atmospheric temperature and carbon dioxide (CO2) concentration and photosynthetically active radiation (PAR) [4]. Previous studies on oil palm have indicated that bunch yield is positively correlated with intercepted radiation per palm. Oil palm is a C3 crop where photosynthesis is directly linked with intercepted radiation to production of sugars through photosynthesis and the Calvin cycle [5], while the photosynthetic rate of individual leaves of all crops with C3 photosynthetic pathways shows a curvilinear relationship with light intensity [6, 7]. According to Corley et al., oil palm is reported to be a source-limited crop at fruiting stage, leading to partitioning between various sinks (fruit, leaf, trunk, and root) of photosynthate to support both vegetative and reproductive growth, with the costs of maintaining the palm being the first call on resources produced by photosynthesis. The photosynthetic rate of young palms increases gradually until two months before the first bunch is harvested. The mesocarp commonly experiences lipid accumulation starting at 14–16 weeks after pollination (WAP)-and takes 22 weeks to ripen fully. The lipid production stage of mesocarp development requires significant demand on carbon sources, such as sugars produced by photosynthesis in the leaves [6, 8]. Understanding limiters of photosynthesis and carbon assimilation in oil palm and any genetic variation that may exist between different populations is therefore important for future crop improvement.

Diurnal light intensities were recorded according to solar radiation at the Dusun Durian Estate weather station for May 2016 (Fig 1). The record showed the light intensity increased above zero at around 07:00 with 7 Wm-2, rising to a maximum of 760 Wm-2 at 14:00. Light intensity then decreased to 0.5 Wm-2 by 20:00. In this study, oil palm leaf samples were collected at five different time points associated with likely boundary points in photosynthetic activity due to light intensity changes throughout the day: 07:00—commencement of photosynthesis; 11:00—near the boundary at the end of the low light morning period; 15:00—at the end of peak light at midday; and 19:00—end of day light intensity minimum before dark. A fifth sampling point was taken at 07:00 the following day to complete a full 24 h diurnal cycle (Fig 1).

Improvement of photosynthetic capacity or activity to increase overall oil palm yield has long been discussed, but to pinpoint the critical rate-limiting processes, we must understand the flow of photosynthesis starting from light interception to gene expression, followed by sugar production and finally the carbon and nitrogen translocation to the mesocarp for oil biosynthesis. As oil palm is a perennial crop, it is challenging to relate short-term cellular processes to long-term oil yield trends, especially comparing leaf biochemical processes and fruit development. The long-term partitioning of carbon and other metabolites between vegetative and reproductive growth can be confounding when attempting to relate instantaneous biochemical or physiological measurements. Moreover, carbon storage in the trunk represents a comparatively large buffer, likely compensating for some of the short-term carbohydrate and starch fluctuations when photosynthesis is insufficient to support immediate plant demand. In an open field, variables such as the number, age, and size of bunches will differ among palms, along with the number of fronds, height and amount of light intercepted. By adopting what is essentially a bulking strategy based on oil yield (the key trait of interest), it is possible to screen for consistent differences between palms in terms of yield performance and fruit characteristics. These differences can be used to identify markers that could potentially be used to screen and select for higher yield.

In this study, the comparison of leaf gas exchange and biochemical observations throughout a diurnal cycle for oil palm groups revealed the significantly faster accumulation of sugar phosphates in HY palms during the period of low light in the morning (between 07:00 and 11:00). This observation was further supported by transcriptome analysis in which 191 DEGs were identified including three photosynthetic genes namely CAB-13, PSI and FNR. All of these genes were found to be significantly expressed in HY palms and could serve as potential biomarkers for the selection of improved planting materials, particularly for conditions of limited light. However, in addition to these, many other DEGs identified were unannotated and would need further validation before being adopted as biomarkers. This discovery of differential photosynthetic machinery and metabolites under low light has important implications for future selection of plants that perform better at peak maturity and with high planting density where light competition may result in yield limitation. In conjunction with the sustainability aim to increase yield per unit of land area, selection of planting materials via photosynthesis-related biomarkers for high-density planting is definitely of significant interest to boost plantation productivity without the need for more land.

 

Source:

http://doi.org/10.1371/journal.pone.0213591

 

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