Expression of Candidate Marker Genes of Sugar Starvation is Enhanced in Growth-Suppressed Parthenocarpic Cucumber Fruit

doi:10.21203/rs.3.rs-1821799/v2

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Expression of Candidate Marker Genes of Sugar Starvation is Enhanced in Growth-Suppressed Parthenocarpic Cucumber Fruit

https://doi.org/10.21203/rs.3.rs-1821799/v2

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Background

In plant, sugar starvation occurs in many stress conditions. Although the involvement plant hormones is known, the underlying mechanism of fruit parthenocarpy is not known. Investigation of sugar starvation in growth suppressed parthenocarpic fruit may shed light on the parthenocarpy mechanism.

Method

Cucumber (Cucumis sativus L.) fruits were followed and harvested at 0, 2, 4, 6, 8 days after anthesis, and the expression of eight candidate marker genes of sugar starvation and sugar concentration were examined.

Results

A growth analysis of fruits showed variability in the onset of exponential growth. Fruits in which growth was suppressed for more than 8 days after anthesis tended to abort. The variation in transcript levels was very high. The correlation matrix of the transcript level of the genes and the time course of the expression of the eight genes led to their classification into three groups. This varying pattern of gene expression may reflect the dynamics of parthenocarpic fruit. Moreover, the gene expression patterns and hexose concentration suggested that sugar starvation occurs in parthenocarpic fruit in which growth is suppressed. Therefore, the asparagine synthetase gene and the Cucumis sativus Somatic Embryogenesis Zinc Finger 1 (CsSEF1), Cucumis sativus Fruit Defoliation Induced 1 (CsFDI1), CsaV3_1G000860, CsaV3_3G041280, and CsaV3_3G023510 genes were regarded as good marker genes of sugar starvation.

Conclusion

The occurrence of sugar starvation suggests the low sink activity precedes the decline in fruit growth. This suggests the sink activity is the control point of parthenocarpic fruit set.

Asparagine synthetase

CsSEF1

Fruit abortion

RNA-seq

New candidate marker genes of sugar starvation in cucumber fruit were obtained.
Sugar starvation suggests low sink activity precedes growth suppression of parthenocarpic cucumber fruit, suggesting that the sink activity is the control point of parthenocarpic fruit set.

Sugar starvation occurs in plant tissues under various stress conditions (Barros et al. 2017; Janse et al. 2019; Slocombe et al. 2004). We searched for marker genes of sugar starvation in cucumber fruit in relation to the development of malformed fruits. Using the subtraction method (Tazuke and Asayama 2013; Tazuke et al. 2015) and RNA-seq analysis (Tazuke et al. 2019), we identified eight candidate genes, including the asparagine synthetase (AS) gene, which is regarded as a very good marker of sugar starvation (Rolland et al. 2006). The function of the remaining genes remains unclear. In a preliminary experiment, the growth cessation of parthenocarpic cucumber fruit was accompanied by the upregulation of the AS, CsSEF1, and CsFDI1 genes, suggesting the occurrence of sugar starvation during the growth cessation or abortion of a fruit (our unpublished data).

Because microspore formation is sensitive to environmental conditions, such as moderate heat stress and low temperature (Mesihovic et al. 2016; Picken 1984; Sato et al. 2006), parthenocarpy is a desired trait. Cucumber has naturally parthenocarpic cultivars. Many reports have shown that parthenocarpy is induced by plant hormones (Fu et al. 2008; Gorguet et al. 2005; Serrani et al. 2010). Moreover, the introduction of the indole-3-acetic acid (IAA)-synthesizing DefH9-iaaM gene in cucumber enhanced parthenocarpy (Yu et al. 2006). In tomato, the overexpression of the auxin-receptor-encoding Solanum lycopersicum transport inhibitor response 1 (SlTIR1) gene (Ren et al. 2011) and the suppression of the expression of the auxin response factor-7 (SlARF7) gene (De Jong et al. 2009) and the Aux/IAA-encoding SlIAA9 gene (Wang et al. 2005) induced parthenocarpy. Parthenocarpy is also induced by gibberellin, and it is suggested that auxin works upstream of gibberellin (Hu et al. 2018; Serrani et al. 2010). However, the direct target of gibberellin remains unknown (Shinozaki et al. 2020). In cucumber, the results of the search for genes responsible for parthenocarpy were equivocal. This may be partly attributed to differences in the measurements of parthenocarpy: Lietzow et al. (2016) used early growth as the measure of the extent of parthenocarpy, whereas Wu et al. (2016) regarded fruits that did not abort as being parthenocarpic, and Sun et al. (2006) used fruit yield as the measure of this trait. Therefore, additional observations of fruit growth and abortion are necessary to address this issue.

The fruits that fail to set eventually abort (Hikosaka and Sugiyama 2004, 2005). It has been suggested that fruit abortion is caused by the source–sink relationship, which triggers sugar shortage in fruit (Marcelis 1993). Thus, the investigation of sugar starvation in parthenocarpic fruit will be informative in this context. In this study, we examined the expression of the candidate marker genes of sugar starvation in association with growth cessation in parthenocarpic cucumber fruit in a moderately parthenocarpic cultivar, as well as in association with fruit growth and sugar concentration, to evaluate the applicability of the candidate genes as markers of sugar starvation.

Plant cultivation and growth analysis of fruits

Cucumber (Cucumis sativus L.) cv. ‘Tokiwa’ plants were grown in a glasshouse. Single plants were grown in 15-L containers filled with vermiculite. The plants were watered every morning with half-strength Hoagland No. 2 solution. Tap water was used to prepare the solution. The plants were de-topped, leaving about 10 leaves. The lateral shoots were pinched, leaving the first node. The female flowers on the first nodes were used for the experiment. In the evening, female flower buds in which the petals had become yellow were judged to flower the next day and were wrapped in a paper bag to prevent pollination. The bag was removed on the day that followed the flowering. In the spring of 2019, fruit length was measured every morning from the day of anthesis until the fruit grew to a marketable size or aborted. In the spring of 2021, fruit length was measured every 2 days from the day of anthesis until 0, 2, 4, 6, and 8 days after anthesis (DAA), when the fruit was harvested. The relative growth rate (in volume) of a fruit (RGR% h^–1) was estimated as follows:

where L0 and L1 are the length of the fruit at the beginning and end of the period of RGR measurement, respectively; and d0 and d1 are the date of the beginning and end of the period, respectively.

Fruit harvest

The harvested fruit was immediately weighed, placed in a jar filled with liquid nitrogen, and transferred to the laboratory. Samples for RNA extraction were stored at –80°C, if necessary, whereas samples for sugar extraction were stored at –30°C.

RNA extraction and reverse transcription

The frozen sample was powdered with a mortar and pestle and total RNA was extracted using the RNeasy Plant Mini Kit (QIAGEN, Hilden). DNA was eliminated with RNase-Free DNase Set (QIAGEN). Finally, the extract was reverse transcribed using the PrimeScript^™ RT reagent Kit (Perfect Real Time) (TaKaRa, Kusatsu) and stored at –30°C.

Real-time PCR

The primers used in this experiment were designed using Primer3web (https://primer3.ut.ee/). The selected reverse transcripts were amplified by PCR. Aliquots of the PCR products were subjected to electrophoresis, to verify the specificity of the primers. The aliquots of the PCR products were subjected to a series of 10-fold dilutions with EASY Dilution (for real-time PCR) (TaKaRa) and used to produce the calibration curve. The genes for which expression was examined are shown in Table 1. Actin was used as the internal standard. Premix Ex Taq^™ (Perfect Real Time) (TaKaRa) was used to perform real-time PCR on a LightCycler^® 96 System (Roche, Basel).

Sugar analysis

The stored frozen samples were powdered with a mortar and pestle, homogenized with 80% ethanol, extracted for 15 min at 80°C, and filled up to 100 mL. Aliquots of 1 mL were dried with a rotary evaporator and redissolved with 1 mL of water, and the concentration of sucrose, glucose, and fructose was analyzed enzymatically using an F-kit (J. K. International, Tokyo).

Statistical analysis

The calculation of the correlation matrix and its visualization were performed using R (R Core Team, 2021).

Our study complies with relevant institutional, national, and international guidelines and legislation.

Fruit growth

Fruit on the day of anthesis is shown in Figure 1a. Fruit at 3 days after anthesis is shown in Figure 1b; at this time point they had not begun exponential growth, which is a typical symptom of growth suppression of parthenocarpic fruit. The growth of fruit based on length is shown in Figure 2a. The onset of exponential growth was set at the time at which RGR became larger than 2% h^–1. Some fruits started to grow exponentially at various DAA, whereas other fruits did not grow exponentially. The distribution of the DAA of the onset of the exponential growth is shown in Figure 2b. About 60% of the fruits did not exhibit exponential growth, and most of them eventually became soft: they were regarded as having aborted. The distribution of the DAA of the fruit abortion is shown in Figure 2c.

Gene expression analysis

At 8 DAA, the levels of the transcripts of all genes were high only in one fruit, and were close to zero in the remaining fruits. This was because most slow fruits aborted, and some slow fruits were larger than the marketable size, in which the RGR decreases normally. Therefore, gene expression was determined from 0 to 6 DAA.

The variation in transcript levels was very large. One possible explanation for this observation is that the extent of the sugar starvation fluctuated greatly among fruits. In this case, the correlation between the transcript level of the genes will be high. The visualized correlation matrix of the genes and RGR at 2–6 DAA is shown in Figure 3. The correlation coefficients (r) of the transcript level of the genes and RGR were moderately negative, with the exception of that obtained for HB (its absolute r value was very low). This negative r was consistent with the relationship between growth cessation and gene expression. The r values among the transcript levels of the AS, CsSEF1, CsFDI1, PMS, and uk4 genes were relatively high, suggesting that these genes are regulated similarly. Remarkably, the r value between CsSEF1 and uk4 and that between CsFDI1 and uk4 were very high.

The variation of the data was much larger than that reported previously (Tazuke and Asayama 2013; Tazuke et al. 2015; Tazuke et al. 2017). The study of the effect of salinity on fruit growth revealed that the RGR of a fruit in which growth was suppressed by salinity tended to fall to about 1.5% h^–1 (Tazuke 1997). Thus, for each DAA, the fruits were classified into two groups: those with an RGR >1.5% h^–1 (referred to as “fast fruit” hereafter), and those with an RGR <1.5% h^–1 (referred to as “slow fruit” hereafter). The average and standard error of each group were calculated. The expression of genes obtained using the subtraction method is shown in Figure 4. The expression of genes obtained by RNA-seq is shown in Figure 5.

For the AS gene, the transcript levels in both fast and slow fruit were high from 2 DAA compared with that observed on the day of anthesis. In slow fruit, the transcript level tended to increase at 6 DAA, whereas in fast fruit, the transcript level decreased markedly. (Fig. 4a).

For the CsSEF1 gene, the transcript level of fast fruit remained low from 0 to 6 DAA. In slow fruit, the transcript level began to increase at 4 DAA and became as high as 50 times the transcript level detected at 0 DAA, although the variance was very large (Fig. 4b).

For the CsFDI1 gene, the pattern of change in transcript levels was similar to that of CsSEF1, although the transcript level of slow fruit at 6 DAA was only about five times the transcript level detected at 0 DAA; however, its variance was very large (Fig. 4c).

For the HB gene, the transcript level increased markedly at 6 DAA. It was higher in fast fruit and about 1000 times higher than the transcript level detected at 0 DAA (Fig. 5a).

For the PMS gene, the transcript level of slow fruit was higher than that of fast fruit and increased with the DAA. The variation in the slow fruit category was very large. The transcript level of fast fruit was relatively high (Fig. 5b).

For the NAC gene, the variability of the slow fruit was very high at 2 DAA and the transcript level of slow fruit was very low at 4 DAA. The transcript level of the slow fruit at 6 DAA was about 200 times the transcript level detected at 0 DAA. The transcript level of fast fruit remained low (Fig. 5c).

For the NA3 gene, the pattern of the change in the transcript level was similar to that of CsSEF1. The transcript level of slow fruit at 6 DAA was about 400 times the transcript level detected at 0 DAA (Fig. 5d).

Finally, for the uk4 gene, the pattern of the change in the transcript level was similar to that of CsSEF1. The transcript level of slow fruit at 6 DAA was about 100 times the transcript level detected at 0 DAA (Fig. 5e).

We identified three patterns of gene expression—type I (AS and PMS), type II (CsSEF1, CsFDI1, NA3, and uk4), and type III (HB and NAC)—based on the time course of gene expression and its correlations.

Sugar levels

In both fast and slow fruit, the sucrose concentration was very low (data not shown). The sum of the concentrations of glucose and fructose was regarded as the hexose concentration and is presented in Figure 6. In fast fruit, hexose concentration was low at 0 DAA and increased steadily with DAA. In slow fruit, hexose concentration became even lower with increasing DAA.

The onset of exponential fruit growth varies considerably. Once exponential growth begins, fruits grow until they reach a marketable size. Thus, the use of the initial growth rate for the parthenocarpy trait may lead to confusion. The source–sink relationship and environmental factors can affect the onset of exponential fruit growth (Hikosaka and Sugiyama 2004, 2005; Marcelis 1993). Fruits that do not commence exponential growth after 8 DAA exhibit a high probability of abortion. Because the suppression of fruit growth is affected by the source–sink relationship and environmental factors, the use of fruit abortion as the indicator of parthenocarpy may not be reliable.

In our previous studies, the expression of the AS, CsSEF1, and CsFDI1 genes in young fruit increased similarly in response to total defoliation, prolonged darkness, salinity, and fruit harvest (Tazuke et al. 2015; Tazuke et al. 2017; Tazuke and Kinoshita 2018). This correlation could explain the difficulty in delineating the causes of gene expression, such as sugar starvation and growth cessation. In the present study, different response patterns in gene expression were observed. This difference may shed light on the triggers of gene expression.

We identified three patterns of gene expression. These genes were identified as the genes that were induced by total defoliation. Therefore, the different patterns of expression of the genes observed during the growth cessation of parthenocarpic fruit are interesting.

The transcript levels of the type I genes were high from 2 DAA in both slow and fast fruit, but were higher in slow fruit. The transcript levels of fast fruit at 6 DAA became close to 0. The fact that AS was the only gene with a known function among the eight genes examined and is regarded as a very good marker of sugar starvation (Rolland et al. 2006) suggests that sugar starvation occurs in young fruit, especially in slow fruit. Moreover, the decrease observed at 6 DAA in fast fruit may reflect the increase in sugar supply. Sugar starvation in fruit may be the result of the decline in sink activity and sugar consumption by the fruit.

If the interpretation provided above is correct, type II genes may not be regarded as marker genes of sugar starvation. The occurrence of fruit abortion depended on DAA. Therefore, it is possible that type II genes are related to fruit abortion. Conversely, AtTZF1, which is a close homolog of CsSEF1, was shown to bind to the target of rapamycin (TOR) mRNA and degrade it (Li et al. 2019). TOR is a central controller of anabolism and is downregulated under nutrient starvation (Rodriguez et al. 2019). Thus, it is also possible that type II genes are markers of sugar starvation. CsSEF1 shows a marked response in fruits under total defoliation and prolonged darkness (Tazuke and Asayama 2013). Therefore, type II genes may be sugar-starvation markers that are specific to fruits.

Type III genes, i.e., HB and NAC, were unlike other genes regarding their expression profile and correlation with other genes. These genes were identified as genes that are induced under total defoliation, similar to other genes (Tazuke et al. 2019). The uniqueness of these genes may reflect the dynamics of parthenocarpic fruit.

Hexose concentration is kept low in slow fruit and is increased in fast fruit. This is consistent with the localization of hexose in vacuoles (Ho 1996); moreover, fruit growth is tightly related to vacuolization (Shinozaki et al. 2020). This clear trend indicates that the rather arbitrary RGR threshold value of 1.5% h^− 1 was practically appropriate. On 0 DAA, vacuolization may have been minimum. Thus, the bulk hexose concentration may have been close to its concentration in the cytosol. This may also have been true in slow fruit, in which extensive vacuolization had not commenced. If this was the case, the marked decline in hexose concentration detected in slow fruit at 4 and 6 DAA may correspond to the occurrence of sugar starvation. This time course of hexose concentration suggests that type II genes are good markers of sugar starvation. It is also possible that moderate sugar starvation occurred even at 2 DAA. This may explain the AS expression pattern observed here. The occurrence of sugar starvation in young normally growing fruit has been suggested (our unpublished data). Thus, it is possible that the difference between type I and type II genes lies in the sensitivity to sugar starvation. The expression of the candidate marker genes of sugar starvation suggests the occurrence of sugar starvation in parthenocarpic fruit. Sugar starvation suggests low sink activity precedes fruit growth suppression, suggesting that the sink activity is the control point of the parthenocarpic fruit set.

The AS, CsSEF1, CsFDI1, PMS (CsaV3_1G000860), NA3 (CsaV3_3G041280), and uk4 (CsaV3_3G023510) genes can be regarded as good marker genes of sugar starvation. The target of parthenocarpic fruit growth is suggested to be sink activity.

Acknowledgement

We thank Dr. Hiroshi Omori of the Graduate School of the University of Tokyo for kind suggestions in statistics.

Ethical approval not applicable

Competing interests The authors declare no competing interests

Authors’ contribution Akio Tazuke planned and supervised the experiment. Kaori Murakami did most of the experiment. Tsuguki Kinoshita helped with R. Tsutomu Kuboyama joined the discussion and helped with the methods. Munehiko Asayama helped writing the manuscript.

Funding not applicable

Data availability

The dataset supporting the conclusions of this article is available from the corresponding author upon reasonable request.

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Table 1 Descriptions of the genes subjected to real-time PCR

¹⁾ Cucurbit Genomics Database Cucumber Chinese Long ver.3

No competing interests reported.

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Expression of Candidate Marker Genes of Sugar Starvation is Enhanced in Growth-Suppressed Parthenocarpic Cucumber Fruit

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Abstract

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Introduction

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Discussion

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