# Impact of drying on the composition and organization tomato fruit cell walls: A biochemical and structural study

Marc Lahaye, Xavier Falourd, Lucie Le Bot, Nadia Bertin, Maja Musse

<figure><img src="image_1.png" /></figure>

## To cite this version:

Marc Lahaye, Xavier Falourd, Lucie Le Bot, Nadia Bertin, Maja Musse. Impact of drying on the composition and organization tomato fruit cell walls: A biochemical and structural study. Food Research International, 2025, 213, pp.116567. 10.1016/j.foodres.2025.116567. hal-05115919

HAL Id: hal-05115919

https://hal.inrae.fr/hal-05115919v1

Submitted on 17 Jun 2025

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_2.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
<figure><img src="image_3.png" /></figure>

# Impact of drying on the composition and organization tomato fruit cell walls: A biochemical and structural study☆

Marc Lahaye<sup>a, *,</sup> Xavier Falourd<sup>a, b</sup>, Lucie Le Bot<sup>a</sup>, Nadia Bertin<sup>c</sup>, Maja Musse<sup>d</sup>

## ARTICLE INFO

### Keywords:

Pectin

Hemicellulose

Cellulose

Water-polysaccharide interactions

Solid-state NMR spectroscopy

## ABSTRACT

The cell walls are known to play an important role in the evolution of tomato quality during processing, but the mechanisms are not always clearly identified. The study investigated changes in cell wall polysaccharides in two tomato varieties, Terradou and H1311, following hot air drying at 45 °C for 18-20 h. Significant reductions in pectic sugars (rhamnose, uronic acid), pectin methyl esterification, and hemicellulose-related sugars (mannose, glucose, xylose) were observed, particularly in H1311, mirroring ripening processes and indicating enzyme activity during drying. Solid-state NMR revealed increase in cellulose crystallinity, especially in Terradou, along with reduced cell wall polysaccharide organization, reduced water content around pectin and increased cell wall interactions of pectin as the fruit dried. The correlations between sugar composition and structural dynamics suggest that mannan may play a key role in cellulose organization. The study highlights the role of fruit genetics and enzymatic breakdown in the drying process. It is hypothesized that preservation of hemicelluloses structure during drying helps maintain cell wall porosity, which may facilitate faster water migration.

## 1. Introduction

Dehydration of fresh fruit and vegetables allows their preservation and easier handling, but it can deteriorate their sensorial, nutritional and sanitary qualities. Several dehydration methods have been developed to mitigate these drawbacks (Jayaraman & Das Gupta, 2020). These methods aim to optimize water diffusion through complex tissues filled with various hygroscopic solutes and across barriers, such as membranes and hydrophilic cell walls (Mujumdar, 2020). Drying is often accompanied by shrinkage and collapse of tissue and cell walls resulting from the reorganization of cells, intercellular spaces and cell wall polymers. This reorganization affects porosity of tissues on the micro- to nanometer scales (Prothon et al., 2003).

At the cell walls scale, these structures are poroviscoelastic assemblies of cellulose, hemicelluloses and pectin, the latter contributing particularly to water retention (Lopez-Sanchez et al., 2020; B. Wang et al., 2023). Pectin is mainly composed of homogalacturonan (HG) and rhamnogalacturonan I (RGI) domains (Lahaye, 2024). HG is partly esterified by methanol at the carboxylic group of its galacturonic acid

backbone, while the alternating rhamnose-galacturonic acid backbone of RGI is partly branched with arabinan, galactan and/arabinogalactan side chains. Hemicelluloses, which are closely associated with cellulose, consist of three polysaccharide families: xyloglucan, glucomannan and xylan, all of which contribute to the porosity of the cell wall network (Lahaye, 2024). Hemicellulose and pectin undergo structural remodeling during plant development, particularly during fruit ripening, which involves cell wall disassembly (Goulao & Oliveira, 2008).

In a previous study, MRI and portable open NMR sensor experiments showed that, among two tomato varieties used for the processing industry, the Terradou variety tended to exhibit a faster hot-air drying kinetic compared to H1311, while the dried products had similar texture and phytonutrient content (Musse et al., 2025). In this study, we hypothesized that cell wall contributed to the different drying kinetics. Cell wall composition, structure and the interaction between water and cell wall polysaccharides were assessed by dynamic solid state variable contact time-cross polarization magic angle spinning <sup>13</sup>C NMR spectroscopy (VCT-CPMAS <sup>13</sup>C NMR). Solid state <sup>13</sup>C NMR spectroscopy has previously revealed the fine structure of cellulose and its interactions

<footnote><sup>a</sup> INRAE, BIA, 44316 Nantes, France</footnote>

<footnote><sup>b</sup> INRAE, BIBS Facility, PROBE Infrastructure, 44316 Nantes, France</footnote>

<footnote><sup>c</sup> INRAE, PSH, 84914 Avignon, France</footnote>

<footnote><sup>d</sup> INRAE, OPAALE, 35044 Rennes, France</footnote>

<footnote>* This article is part of a Special issue entitled: 'Magnetic Resonance in Food Science' published in Food Research International.</footnote>

<footnote>* Corresponding author: UR BIA, INRAE, 3 impasse Yvette Cauchois, CS 71627, 44316 Nantes, France.
E-mail address: marc.lahaye@inrae.fr (M. Lahaye).</footnote>
with pectin in primary-type cell wall (T. Wang & Hong, 2016; White et al., 2014). The VCT-CPMAS ¹³C NMR experiment provides access to proton magnetization diffusion times to carbon (TCH, THH) and proton relaxation time (T1p), which offer nanometric-scale information on the proximity of hydrogen-containing compounds, such as water, and the ordering around carbons, such as cellulose crystallinity (Falourd et al., 2022a; Falourd et al., 2024). These parameters have previously shown that cellulose-pectin organization and pectin hydration distinguish the viscoelastic properties of apple flesh, influencing firmness and softening during ripening (Lahaye et al., 2020; Lahaye et al., 2023). In the present case, these parameters were investigated to assess the nanoscale organization underlying the different drying kinetics of the two tomato varieties.

## 2. Materials and methods

### 2.1. Fruits

Tomato (Solanum lycopersicum) fruits of two industrial cultivars (H1311 and Terradou) were produced in a greenhouse at INRAE Avignon in spring 2023. Equatorial slices (24 mm height), free of core, locular tissue and seeds, of similar color and size were analyzed by MRI in a previous study both in the fresh state and after hot-air oven drying (45 °C). Drying was realized according to (Musse et al., 2025). Briefly, tomato slices were placed on a 10 mm mesh grid in the ventilated oven at 45 °C (Froilabo AP120, France) and left for different times to reach targeted residual water content. The samples studied are the batch 1 samples analyzed by MRI in (Musse et al., 2025). The fresh fruit water content was 92.3 ± 0.8 % (n = 5) for H1311 and 92.1 ± 0.9 % (n = 5) for Terradou. Terradou was dried 18 h, resulting in a residual water content of 43.6 ± 11.9 % (n = 5), while H1311 was dried for 20.4 ± 3.0 h to reach a final water content of 49.6 ± 8.1 %, (n = 5). The fresh and partially dried slices were freeze-dried, ground in liquid nitrogen (Spex sample prep freezer mill 6770, Metuchen, NJ, USA), and the resulting powder was dried in vacuo over P2O5 at 40 °C.

### 2.2. Cell wall preparation

Cell wall material was prepared as alcohol insoluble material (AIM) from dried cryomilled tomato powders with an automated solvent extractor (ASE 200, Thermo Scientific, USA) as reported (Minoia et al., 2016). Seventy percent ethanol extracted powders were further processed with 96 % ethanol and acetone prior to air drying and then at 40 °C in vacuo over P2O5. Recovered powders were further ground in a ball mill (FastPrep, MP Biomedicals, USA) at a speed of 6.5 m.s⁻¹ for 20 s prior to further analyses.

### 2.3. Cell wall composition

#### 2.3.1. Neutral sugar content in AIM

Neutral sugar composition in AIM was determined after sulfuric acid pre-hydrolysis and hydrolysis, reduction and acetylation of the monomers according to (Minoia et al., 2016). The alditol acetates were identified and quantified by gas chromatography (Perkin Elmer Clarus 580, USA; column Trace Gold 225 MS ThermoScientific, USA) according to (Minoia et al., 2016). Inositol was used as an internal standard.

#### 2.3.2. Uronic acid content in AIM

Uronic acid content was determined by colorimetry from the acid hydrolysate of the neutral sugar composition analysis according to (Blumenkrantz & Asboe-Hansen, 1973).

#### 2.3.3. Methyl esterification of pectin and variation in protein content in AIM

Methyl esterification of pectin and protein content variation in AIM

dry powders was determined by FTIR (Nicolet iS50 FT-IR, Thermo Scientific, USA) using an ATR device (Smart iTX, ThermoScientific). Spectra were registered (128 scans) between 4000 and 400 cm⁻¹ (resolution 4 cm⁻¹). FTIR Spectra were analyzed using the library ChemoSpec on R (Hanson, 2022).

Degree of methyl esterification of pectin (DM) was measured by the ratio of the band at 1740 cm⁻¹ (ester carbonyl group stretching) to the sum of the intensities of the peaks at 1740 and 1630 cm⁻¹ (carboxylate group stretching) x 100 (Kyomugasho et al., 2015). This ratio corresponds to the percentage of methyl esterified uronic acid.

Variation in protein content was assessed by comparing the area of the absorbances between 1500 and 1550 cm⁻¹ for amide II to the area of absorbances of polysaccharides (1190–840 cm⁻¹) (Andrade et al., 2019).

### 2.4. Solid-state NMR analyses

#### 2.4.1. Cross polarization magic angle spinning ¹³C NMR spectra (CPMAS)

Solid-state NMR spectroscopy was realized on a Bruker NEO 400 Ascend WB spectrometer operating at a proton frequency of 400.15 MHz and a carbon frequency of 100.63 MHz. A double resonance ¹H/X CPMAS 4 mm probe connected to a high power-level amplifier was used. The magic angle spinning (MAS) rate was set at 12 kHz and each acquisition was acquired at regulated temperature (293 K). Chemical shifts were calibrated with external glycine, assigning the carbonyl at 176.03 ppm.

#### 2.4.2. MultiCPMAS ¹³C NMR spectra and cellulose crystallinity measurement

MultiCPMAS spectra (Johnson & Schmidt-Rohr, 2014) was acquired using seven contact blocks separated by repolarization periods (tz) of 0.9 s. Experiments were conducted using a 90° proton pulse of 4.0 +/− 0.3 µs. The chemical shifts, half width and area of peak of samples were determined using a least-squares fitting method with the Peakfit® software (Systat software Inc., USA). The percentage cellulose crystallinity was determined with the peak area ratio of two lines for the crystalline part (88.2 +/− 0.3 and 86.6 +/− 0.4 ppm)/three lines for the cellulose C-4 region including 83.5 +/− 0.3 ppm associated to amorphous cellulose x 100. The percentage degree of methyl-esterification of pectin was determined with the peak area ratio of the two lines for COOCH3 (170.6 +/− 0.4 ppm) / to the lines for carboxylic region (174.6 +/− 0.4, 172.2 +/− 0.2 and 170.6 +/− 0.4 ppm) x 100.

#### 2.4.3. Dynamic solid-state NMR: Variable contact time-CPMAS ¹³C NMR spectra (VCT-CPMAS)

The VCT-CPMAS ¹³C NMR spectra were based on the “classical” CPMAS pulse sequence in which the contact time was varied. Based on our previous work, a kinetics of 173 contact times using 128 accumulations with a recovery time of 3 s was selected (Falourd et al., 2022b). The distribution of the contact times increased step-wise between 5 and 10,000 µs, with 5 µs steps from 5 to 130 µs, 10 µs steps from 130 to 1000 µs, 50 µs steps from 1000 to 2000 µs, and 200 µs steps from 2000 to 10,000 µs. The overall acquisition time was 21 h per sample.

Different levels of simplification on the equation used for modeling can be applied. This was evaluated as previously (Falourd et al., 2022a) and led to the choice of the following one: The complex two-proton reservoir model with anisotropic spin diffusion for polysaccharide signals (sum of C1 to C5):

$$I(\tau) = I_0 e^{-\tau/T_{1p}^H} \left( 1 - \lambda e^{-\tau/T_{HHa}} - (1 - \lambda)e^{-\tau/T_{HHc}} \times e^{-\tau^2/2T_{CH}^2} \right)$$

Where I(τ) is the signal intensity at time τ, T1p is the spin-lattice relaxation time in the rotating frame which increases with the level of molecular order. THHa and THHc are the spin diffusion times characterizing strong H–H couplings. Previous work suggests that THHc
decreases with water penetration into the cellulose network. TCH is associated with the heteronuclear H—C coupling and could be associated with macromolecular interaction as shown by its relation with the second dipole moment M2 (Kolodziejski & Klinowski, 2002).

Two-proton reservoir model with isotropic spin diffusion for the methyl signal of the pectin methyl ester:

$$I(\tau) = I_0 e^{-\tau/T_{1p}^H} \left( 1 - \lambda e^{-\tau/T_{HH}} - (1 - \lambda)e^{-3\tau/2T_{HH}} \times e^{-\tau^2/2T_{CH}^2} \right)$$

This is a simplified version of the previous equation considering the spin diffusion phenomenon as isotropic.

NMR analysis were realized on three biological repeats for each variety and drying condition.

## 2.5. Statistics

Sugar content analyses, DM and protein variation estimates were determined on five biological repeats per variety and drying condition, three FTIR spectra were registered per biological repeat.

Statistical analyses were realized on R (R Core Team, 2024). Kruskal Wallis non-parametric test followed by Dunn post hoc test were realized on data. Non-parametric Spearman correlations were realized taking the available composition and NMR data from the three selected tomato samples per variety and drying status.

# 3. Results and discussion

The sugar composition and the degree of methyl esterification of pectin were determined in the AIM from both fresh and partially dried tomato fruits (Fig. 1). The values were consistent with published data (Broxterman & Schols, 2018; Devaux et al., 2005; Orfila et al., 2002;

<figure><img src="image_4.png" /><figcaption>Fig. 1. Sugar composition and degree of methyl esterification of pectin (values means ± standard deviation, n = 5) of AIM from H1311 (H) and Terradou (T) at the fresh (f) stage and after partial drying (d). Different lowercase letters indicate significant differences between fresh and dried fruit within each variety; different capital letters indicate significant differences between varieties at the same drying stage, p ≤ 0.05.</figcaption></figure>
Sinkora et al., 2024; Van Audenhove et al., 2021) and showed a sig-
nificant decrease in pectic sugars (rhamnose, uronic acid) and
hemicellulose/cellulose-related sugars, such as mannose, glucose and
xylose, particularly in H1311, after drying (Fig. 1). Considering specif-
ically the pectin and cellulose/hemicellulose compositions (mol%
basis), there are no significant differences between the varieties at each
stage (Fig. 2 HC and RGI). The only change was the increase in the
cellulose and hemicellulose content in dried samples due to the decrease
in pectin content, particularly in the HG domains. The contents of
arabinose and galactose, which are present in pectic RGI side chains,
hemicelluloses (xyloglucan and glucomannans), and arabinogalactan
proteins, are differently impacted by drying: dried Terradou contained
significantly more arabinose than galactose compared to H1311 (Fig. 2
Ara/Gal). This difference may be attributed to a higher content of ara-
binosylated hemicelluloses, such as xyloglucan and/or glucomannan
(Assor et al., 2013), or to a reduced degradation of arabinogalactan
proteins, which has been reported to occur during tomato ripening
(Kutyrieva-Nowak et al., 2023). The ratio of the sum of galactose and
arabinose mol% to that of rhamnose, often used to assess the length of
RGI branching, shows no significant differences between varieties and
drying conditions (Fig. 2 (Gal+Ara)/Rha). This result suggests that,
wherever arabinose and galactose are located, their global molar pro-
portion does not change significantly in relation to the RGI backbone
during fruit drying, indicating that their metabolism is similar in Ter-
radou and H1311.

The two varieties also exhibited a similar decrease in pectin linearity
after drying, likely due to greater metabolism of the HG pectic domain
(Fig. 2 UA/Rha). These compositional features of pectin contrast with
previously reported values from the purée of same tomato varieties
(Sinkora et al., 2024), likely reflecting differences in the ripening status
of the fruits studied in those reports. A notable decrease in the degree of

pectin methyl esterification was also observed (Fig. 1).

These results clearly established that cell wall modifications
occurred during tomato drying, reminiscent of changes that take place
during fruit ripening (Goulao & Oliveira, 2008; Toivonen & Brummell,
2008; D. Wang et al., 2018). These include substantial reduction in total
sugar content in the AIM, as previously observed during tomato ripening
to the benefit of proteins (Devaux et al., 2005). In line with these results,
a significant increase in the FTIR amide II absorbance between 1500 and
1550 cm⁻¹ with regard to the carbohydrate absorbances between 840
and 1190 cm⁻¹ was observed for the two varieties after drying (Fig. 3).
These findings suggest that endogenous enzyme, particularly pectino-
lytic enzymes, were active during hot air drying at 45 °C. In fact, the
inhibition of endogenous enzymes requires much higher temperatures,
and some, such as pectin methyl esterase, may have been activated
(Anthon et al., 2002; Anthon & Barrett, 2006; Crelier et al., 2001; Fachin
et al., 2003). As a result, cell wall polysaccharides, particularly pectin,
were broken down into oligomers and monomers which were metabo-
lized and/or, most likely, lost during AIM preparation, leading to lower
recovery in cell wall polysaccharides. The higher weight percentage of
glucose, xylose and mannose in the partially dried Terradou samples
compared to H1311 likely reflects varietal differences in the activity of
endogenous enzymes, such as xyloglucan- and mannan-
transglycosylase/hydrolase, which are known to contribute to cell
wall disassembly during fruit ripening (Frankova & Fry, 2013). These
variations are consistent with the fact that changes in composition and
structure of tomato hemicellulose during ripening are influenced by
genetics (Lahaye et al., 2012).

To get a better insight into the role of the structure and organization
of the cell wall polysaccharides in the differential drying kinetics be-
tween Terradou and H1311, multi-CPMAS- and VCT CPMAS-¹³C NMR
spectroscopic analyses were conducted on three arbitrarily selected

<figure><img src="image_5.png" /><figcaption>**Fig. 2.** Proportions of cellulose and hemicellulose (HC = sum of glucose, mannose, xylose mol%) and rhamnogalacturonan I (RGI = sum of 2 x rhamnose, galactose, arabinose mol%) and mol% ratio of arabinose and galactose (Ara/Gal), uronic acid and rhamnose (UA/Rha) and the sum of galactose and arabinose mol% per rhamnose (Gal/Ara/Rha) of AIM from H1311 (H) and Terradou (T) at the fresh (f) stage and after partial drying (d). Bars represent standard deviations (n = 5); different lowercase letters indicate significant differences between fresh and dried fruit within the variety; different capital letters indicate significant differences between varieties at the same drying stage, p ≤ 0.05.</figcaption></figure>
<figure><img src="image_6.png" /><figcaption>**Fig. 3.** Ratio of the amide II absorbances (area under the 1500–1550 cm⁻¹ region) for protein to those of polysaccharides (area under the 1190–840 cm⁻¹ region) in the FTIR of AIM from H1311 (H) and Terradou (T) at the fresh (f) stage and after partial drying (d). Bars represent standard deviations (n = 5); different lowercase letters indicate significant differences between fresh and dried fruit within each variety, *p* ≤ 0.05.</figcaption></figure>

samples AIMs of fresh and partially dried fruits. The quantitative multi-CPMAS ¹³C NMR spectra showed close overall structure and composition of the cell wall polysaccharides in AIM of the fresh H1311 and Terradou (Fig. 4). The chemical shifts observed corresponded to those of cellulose, hemicellulose and pectin (Hediger et al., 1999; Rondeau-Mouro et al., 2003; White et al., 2014), along with signals between 23 and 32 ppm for aliphatic carbons, such as those found in amino acids and particularly in the epidermal surface polyester, cutin (Chatterjee et al., 2016). Aromatic signals associated with polyphenols or amino acids were observed in the range of 110 to 160 ppm. Cellulose crystallinity was around 35 to 40 %, and tended to increase after drying, particularly for Terradou, where this increase was significant, rising from 35.3 to 38.9 % (*p* < 0.05; supplementary Table S1). Upon partial drying, differences were also noted at around 170–175 ppm, indicating a decrease in methyl esterified carboxylic acid (170 ppm) in favor of the de-esterified form (Phyo et al., 2017). This effect was more pronounced in H1311 than in Terradou (supplementary Table S1), which aligns well with DM values measured by FTIR (Fig. 1). Along with pectin de-esterification, which was also evidenced from the marked decrease in the methyl carbon signal at 53 ppm, a lower proportion of pectin and hemicellulose in the AIM of partially dried tomatoes was observed. This was reflected by the reduced intensity of carbon signals at around 95–100 and 78–80 ppm, corresponding to C1 and C4 in pectin and hemicellulose (Fig. 4).

The evolution of the cell wall structure at the nanometric scale during the drying process was evaluated by analyzing the dynamics of proton magnetization diffusion to carbon using VCT-CPMAS ¹³C NMR. Due to time constraints on data acquisition, samples AIM from three different fruits at both fresh and drying stages were analyzed. By using increasing contact times for proton magnetization transfer to carbon, a curve of carbon signal intensity was generated (Fig. 5). The raising part of the curve mostly reflects the direct transfer of magnetization from protons attached to carbon (T<sub>CH</sub>) and the diffusion time of magnetization from hydroxyl and surrounding water protons to carbon (T<sub>HH</sub>). The declining part of the curve primarily reflects proton relaxation time

(T<sub>1p</sub><sup>H</sup>). Longer diffusion or relaxation times indicate more numerous or similar structures surrounding the probed carbon atoms. Long T<sub>CH</sub> values reflect closely interacting polysaccharide chains (Kolodziejski & Klinowski, 2002), and their duration is reduced by water (Falourd et al., 2024); long T<sub>HH</sub> values indicate numerous hydrogen atoms from water or hydroxyl groups near the carbon (Hediger et al., 1999), while long T<sub>1p</sub><sup>H</sup> values are associated with a highly ordered environment; in the case of cellulose, this is related to crystallinity (Falourd et al., 2022a).

Different equations can be applied to extract these parameters from the curve (Falourd et al., 2022a). In this study, a model of two proton reservoirs with anisotropic spin diffusion was used to analyze the curve derived from cumulative C1-C5 signals, which combine cellulose, pectin and hemicellulose signals to ensure sufficient signal intensity and reduced noise. This model provides more detailed information on water-polysaccharide interactions through distinct T<sub>HH</sub> diffusion times, such as T<sub>HHa</sub> and T<sub>HHc</sub>. T<sub>HHa</sub> corresponds to very close interactions between water protons and cellulose (< 1 nm), while T<sub>HHc</sub> is associated with water-sensitive protons of hydroxyl groups (~30 nm) (Falourd et al., 2022a). When individual signals were used to build the curve, such as for the pectin methyl ester (~53.5 ppm), the pectin carbonyl signal (~173 ppm), or the major signal of cutin (~28 ppm), the noisiness of the curve, especially at short and long contact times, required a more generalized model with a single proton reservoir.

The mean spin diffusion and relaxation data of AIM from fresh and partially dried fruits are shown in Fig. 6 and in the supplementary Table 2 (Table S2). The drying process, along with associated ripening, significantly reduced the organization of cell wall polysaccharides (T<sub>1p</sub><sup>H</sup>), decreased water content around pectin (T<sub>HHpectin</sub>), and increased interactions of pectin chains (T<sub>CHpectin</sub>) with surrounding polymers. The decrease in T<sub>1p</sub><sup>H</sup> during tomato ripening and highly mobile pectin agree with previous results (Fenwick et al., 1996). The cutin environment and hydration of cell wall polysaccharides within the cuticle did not appear to be markedly affected by the drying process, although non-significant trends toward lower T<sub>HHc</sub> and T<sub>CH</sub> were observed (Table S2). These trends suggest a possible modulation of water content around cutin and cell wall polysaccharides embedded in cutin polymers (Reynoud et al., 2022). Regarding varietal differences, only the T<sub>1p</sub><sup>H</sup> values of the AIM from H1311 showed a significant decrease after partial drying of the fruit (from 8.8 ± 0.2 to 6.3 ± 1.5 ms), while Terradou's value remained stable (9.1 ± 2.1 and 8.6 ± 0.2 ms). This is consistent with the observation that cell wall composition of H1311 is more impacted by the drying than that of Terradou.

Correlation were sought between the biochemical composition of the AIM from all fruit and the NMR dynamic parameters (Fig. 7). In addition to the expected correlations, for instance between pectin methyl esterification and uronic acid and total sugar content, a noteworthy positive correlation was found between T<sub>1p</sub><sup>H</sup> and the mannose and total sugar contents (*p* ≤ 0.01). This suggests that mannose-containing structure (mannan, glucomannan hemicelluloses) contributes to the organization of cell wall polysaccharides (Fig. 8A). In wood, mannan/glucomannans coat cellulose fibers at the interface with xylan and lignin (Berglund et al., 2020). In tomato fruit, glucomannan may also play a role in organizing cellulose fibers. Its metabolism along with that of xyloglucan occurring during fruit ripening, likely disrupts the environment around cellulose fibers with an effect on cell wall polysaccharides ordering and T<sub>1p</sub><sup>H</sup>.

The correlation between total sugar content and the ordering of cell wall polysaccharides likely reflects the overall disassembly and metabolism of the cell wall during drying, leading to an impoverishment in polysaccharides (Fig. 8B). Further correlation between mannose and rhamnose content suggests co-occurring metabolism of mannan/glucomannan and RGI pectic structures during drying.

Another significant finding was the positive correlation of T<sub>HHpectin</sub> with uronic acid content, DM and TS (*p* ≤ 0.01) (Fig. 7), which is closely related with the ripening process during partial drying (Fig. 8D, E). The high proton density around pectin due to its hydrophilic nature has
<figure><img src="image_7.png" /><figcaption>**Fig. 4.** Multi-CPMAS ¹³C NMR spectra of AIM from three different fresh (f) and partially dried (d) Terradou (T) and H1311 (H) fruits. Carbon 1 to 6 (C1–6) were attributed to cell wall polymers and more specifically to cellulose (C4cr, C6cr), pectin (COOH/COOR, OMe), hemicellulose and cutin (C aliphatic). Traces of aromatic C are also noted. Areas shaded in grey on the spectra correspond to signals affected by the drying process. The area of the spectra has been normalized to the weight of AIM in the rotor. Different color spectra correspond to different fruits.</figcaption></figure>

<figure><img src="image_8.png" /><figcaption>**Fig. 5.** Kinetics of C1 to C5 ¹³C signal intensity according to contact time in the VCT-CPMAS experiment on AIM material recovered from fresh (f) and partially dried (d) Terradou (T) and H1311 (H) tomatoes. Different colors correspond to different fruits.</figcaption></figure>

previously been reported in onion (Hediger et al., 1999). The decrease in T<sub>HHpectin</sub> with ripening, along with the reduction in uronic acid content, which greatly contributes to TS, and the degree of methyl esterification of pectin, reflects a diminished interaction/proximity of water around the remaining pectin. A decrease in T<sub>HHpectin</sub> has also been observed during apple softening in storage, indicating a redistribution of water

within the cell wall as disassembly progresses (Lahaye et al., 2023). For these correlations related to ripening (T<sub>1p</sub><sup>H</sup>, T<sub>HHpectin</sub>), no significant differences were found between the two tomato varieties.

Other weak correlations (p ≤ 0.05) were observed between T<sub>HHc</sub>-TS, Man-TS and Xyl-Glc (Fig. 7). These findings suggest positive local interaction between water and cell wall polysaccharides (T<sub>HHC</sub>), mannose content as an indicator of total sugar content, and a correlation between xylose and glucose, consistent with the presence of xyloglucan in the fruits AIM.

## 4. Conclusion

Hot-air drying at 45 °C for 18–20 h of Terradou and H1311 tomato varieties led to ripening-related cell wall disassembly, particularly affecting pectin content. At the nanometric scale, dried products exhibited significant disorganization of cell wall polysaccharides (lower T<sub>1p</sub><sup>H</sup>), a reduced amount of water surrounding residual pectin (lower T<sub>HHpectin</sub>), and an increase in pectin-chain interactions (increased in T<sub>CHpectin</sub>), supporting the observation of partially dehydrated and collapsed cell walls. While the two varieties shared similar overall cell wall composition in the fresh state, significant differences in the content in arabinose, mannose, xylose, glucose in the dried products revealed distinct, genetically defined cell wall disassembly mechanisms in Terradou and H1311. Given the trend for faster drying process in Terradou compared to H1311 (Musse et al., 2025), the preserved ordering of cell
<figure><img src="image_9.png" /><figcaption>**Fig. 6.** Statistically significant dynamic VCT-CPMAS ¹³C NMR parameters (different letters: $p \le 0.05$) distinguishing AIM from fresh (f) and partially dried (d) tomatoes (combined Terradou and H1311 data). Numbers correspond to mean ± standard deviation, *n* = 6.</figcaption></figure>

<figure><img src="image_10.png" /><figcaption>**Fig. 7.** Correlation plot (Spearman, $p \le 0.05$) between NMR and biochemical data from the combined results from AIM of fresh and partially dried Terradou and H1311.</figcaption></figure>

wall polysaccharide in Terradou and the correlation between $T_{1\rho}^H$ and mannose content suggest that the conservation of the cellulose-hemicellulose network during drying facilitates water transport through cell wall nanopores. Further work is needed to establish the role of osmolytes and secondary metabolites, along with the breakdown of cells and organelles, in the diffusion of water through the fruit matrix and cell wall during the drying process.

These results provide insights into potential cell wall-related genetic and biochemical markers for the selection of tomato varieties and other fleshy fruits for improved drying efficiency, ultimately leading to energy

savings.

### CRediT authorship contribution statement

**Marc Lahaye:** Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Methodology, Investigation, Conceptualization.
**Xavier Falourd:** Writing – review & editing, Visualization, Validation, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.
**Lucie Le Bot:** Visualization, Validation, Methodology, Investigation, Formal analysis, Data curation,
<figure><img src="image_11.png" /><figcaption>**Fig. 8.** Regression lines between NMR and biochemical data from the combined results from AIM of Terradou and H1311 fresh (green) and partially dried (red). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)</figcaption></figure>

**Conceptualization.** Nadia Bertin: Writing – review & editing, Supervision, Conceptualization. Maja Musse: Writing – review & editing, Project administration, Funding acquisition, Conceptualization.

**Declaration of competing interest**

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

**Acknowledgements**

The authors thank the technical assistance of Didier Anato (INRAE, A2M, 84914 Avignon, France) and Valérie Serra (INRAE, PSH) for their experimental support in tomato fruit production, Mireille Cambert, Clémentine Lorho and Yves Diascorn for the handling and preparation of samples (sampling of fruit, drying of fruit slices, freeze-drying and samples management).

**Appendix A. Supplementary data**

Supplementary data to this article can be found online at https://doi.org/10.1016/j.foodres.2025.116567.

**Data availability**

Data will be made available on request.

**References**

Andrade, J., Pereira, C. G., Almeida Junior, J. C. D., Viana, C. C. R., Neves, L. N. D. O., Silva, P. H. F. D., ... Anjos, V. D. C. D. (2019). FTIR-ATR determination of protein content to evaluate whey protein concentrate adulteration. *Lwt*, 99, 166-172.
https://doi.org/10.1016/j.lwt.2018.09.079

Anthon, G. E., & Barrett, D. M. (2006). Characterization of the temperature activation of pectin Methylesterase in green beans and tomatoes. *Journal of Agricultural and Food Chemistry*, *54*, 204-211. https://doi.org/10.1021/jf051877q

Anthon, G. E., Sekine, Y., Watanabe, N., & Barrett, D. M. (2002). Thermal inactivation of pectin Methylesterase, Polygalacturonase, and peroxidase in tomato juice. *Journal of Agricultural and Food Chemistry*, *50*, 6153-6159. https://doi.org/10.1021/jf020462r

Assor, C., Quemener, B., Vigouroux, J., & Lahaye, M. (2013). Fractionation and structural characterization of LiCl-DMSO soluble hemicelluloses from tomato. *Carbohydrate Polymers*, *94*(1), 46-55. https://doi.org/10.1016/j.carbpol.2013.01.001

Berglund, J., Mikkelsen, D., Flanagan, B. M., Dhital, S., Gaunitz, S., Henriksson, G., ... Vilaplana, F. (2020). Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks. *Nature Communications*, *11*(1), 4692.
https://doi.org/10.1038/s41467-020-18390-z

Blumenkrantz, N., & Asboe-Hansen, G. (1973). New method for quantitative determination of uronic acids. *Analytical Biochemistry*, *54*(2), 484-489. https://doi.org/10.1016/0003-2697(73)90377-1

Broxterman, S. E., & Schols, H. A. (2018). Interactions between pectin and cellulose in primary plant cell walls. *Carbohydrate Polymers*, *192*, 263-272. https://doi.org/10.1016/j.carbpol.2018.03.070

Chatterjee, S., Matas, A. J., Isaacson, T., Kehlet, C., Rose, J. K., & Stark, R. E. (2016). Solid-state (13)C NMR delineates the architectural Design of Biopolymers in native and genetically altered tomato fruit cuticles. *Biomacromolecules*, *17*(1), 215-224.
https://doi.org/10.1021/acs.biomac.5b01321

Crelier, S., Robert, M.-C., Claude, J., & Juillerat, M.-A. (2001). Tomato (Lycopersicon esculentum) pectin Methylesterase and Polygalacturonase behaviors regarding heat- and pressure-induced inactivation. *Journal of Agricultural and Food Chemistry*, *49*, 5566-5575. https://doi.org/10.1021/jf010202u

Devaux, M.-F., Barakat, A., Robert, P., Bouchet, B., Guillon, F., Navez, B., & Lahaye, M. (2005). Mechanical breakdown and cell wall structure of mealy tomato pericarp tissue. *Postharvest Biology and Technology*, *37*, 209-221. https://doi.org/10.1016/j.postharvbio.2005.04.013

Fachin, D., Van Loey, A. M., Ly Nguyen, B., Verlent, I., Indrawati, & Hendrickx, M. E. (2003). Inactivation kinetics of polygalacturonase in tomato juice. *Innovative Food
Science & Emerging Technologies, 4(2), 135-142. https://doi.org/10.1016/S1466-8564(02)00090-5

Falourd, X., Lahaye, M., & Rondeau-Mouro, C. (2022a). Assessment of cellulose interactions with water by ssNMR: (1)H->(13)C transfer kinetics revisited. *Carbohydrate Polymers*, 298, Article 120104. https://doi.org/10.1016/j.carbpol.2022.120104

Falourd, X., Lahaye, M., & Rondeau-Mouro, C. (2022b). Optimization of acquisition and processing times for the measurement of 1H to 13C polarization transfer kinetics. *MethodsX*, 9. https://doi.org/10.1016/j.mex.2022.101914

Falourd, X., Rondeau-Mouro, C., Cambert, M., Lahaye, M., Chabbert, B., & Aguié-Béghin, V. (2024). Assessing the complementarity of time domain NMR, solid-state NMR and dynamic vapor sorption in the characterization of polysaccharide-water interactions. *Carbohydrate Polymers*, 326, Article 121579. https://doi.org/10.1016/j.carbpol.2023.121579

Fenwick, K. M., Jarvis, M. C., Apperley, D. C., Seymour, G. B., & Bird, C. R. (1996). Polymer mobility in cell walls of transgenic tomatoes with reduced polygalacturonase activity. *Phytochemistry*, 42(2), 301-307. https://doi.org/10.1016/0031-9422(95)00873-X

Frankova, L., & Fry, S. C. (2013). Biochemistry and physiological roles of enzymes that "cut and paste" plant cell-wall polysaccharides. *Journal of Experimental Botany*, 64 (12), 3519-3550. https://doi.org/10.1093/jxb/ert201

Goulao, L. F., & Oliveira, C. M. (2008). Cell wall modifications during fruit ripening: When a fruit is not the fruit. *Trends in Food Science and Technology*, 19, 4-25. https://doi.org/10.1016/j.tifs.2007.07.002

Hanson, B. A. (2022). *ChemoSpec: Exploratory Chemometrics for spectroscopy. In (R package version 6.1.3 ed.).*

Hediger, S., Emsley, L., & Fischer, M. (1999). Solid-state NMR characterization of hydration effects on polymer mobility in onion cell-wall material. *Carbohydrate Research*, 322, 102-112. https://doi.org/10.1016/S0008-6215(99)00195-0

Jayaraman, K. S., & Das Gupta, D. K. (2020). Drying of fruits and vegetables. In A. S. Mujumdar (Ed.) (Second Ed. ed., Vol. 1. Handbook of industrial drying (pp. 643-690). CRC.

Johnson, R. L., & Schmidt-Rohr, K. (2014). Quantitative solid-state 13C NMR with signal enhancement by multiple cross polarization. *Journal of Magnetic Resonance*, 239, 44-49. https://doi.org/10.1016/j.jmr.2013.11.009

Kolodziejski, W., & Klinowski, J. (2002). Kinetics of cross-polarization in solid-state NMR: A guide for chemists. *Chemical Reviews*, 102(3), 613-628. https://doi.org/10.1021/cr000060n

Kutyrieva-Nowak, N., Leszczuk, A., Zając, A., Kalaitzis, P., & Zdunek, A. (2023). Arabinogalactan protein is a molecular and cytological marker of particular stages of the tomato fruit ripening process. *Scientia Horticulturae*, 310. https://doi.org/10.1016/j.scienta.2022.111718

Kyomugasho, C., Christiaens, S., Shpigelman, A., Van Loey, A. M., & Hendrickx, M. E. (2015). FT-IR spectroscopy, a reliable method for routine analysis of the degree of methylesterification of pectin in different fruit- and vegetable-based matrices. *Food Chemistry*, 176, 82-90. https://doi.org/10.1016/j.foodchem.2014.12.033

Lahaye, M. (2024). Texture of vegetable and fruit. In A. Rosenthal, & J. Chen (Eds.), *Food Texturology: Measurement and perception of food textural properties* (pp. 265-289). Springer Nature. https://doi.org/10.1007/978-3-031-41900-3.

Lahaye, M., Falourd, X., Laillet, B., & Le Gall, S. (2020). Cellulose, pectin and water in cell walls determine apple flesh viscoelastic mechanical properties. *Carbohydrate Polymers*, 232, Article 115768. https://doi.org/10.1016/j.carbpol.2019.115768

Lahaye, M., Quemener, B., Causse, M., & Seymour, G. B. (2012). Hemicellulose fine structure is affected differently during ripening of tomato lines with contrasted firmness. *International Journal of Biological Macromolecules*, 51(4), 462-470. https://doi.org/10.1016/j.ijbiomac.2012.05.024

Lahaye, M., Thoulouze, L., Calatraba, M., Gauclain, T., Falourd, X., Le-Quere, J. M., ... Bauduin, R. (2023). A multimodal and multiscale investigation of factors affecting the juice yield of cider apples. *Food Chemistry*, 420, Article 135649. https://doi.org/10.1016/j.foodchem.2023.135649

Lopez-Sanchez, P., Martinez-Sanz, M., Bonilla, M. R., Sonni, F., Gilbert, E. P., & Gidley, M. J. (2020). Nanostructure and poroviscoelasticity in cell wall materials

from onion, carrot and apple: Roles of pectin. *Food Hydrocolloids*, 98. https://doi.org/10.1016/j.foodhyd.2019.105253

Minoia, S., Boualem, A., Marcel, F., Troadec, C., Quemener, B., Cellini, F., Petrozza, A., Vigouroux, J., Lahaye, M., Carriero, F., & Bendahmane, A. (2016). Induced mutations in tomato SExp1 alter cell wall metabolism and delay fruit softening. *Plant Science*, 242, 195-202. https://doi.org/10.1016/j.plantsci.2015.07.001

Mujumdar, A. S. (2020). *Handbook of industrial drying* (2nd ed.) (2nd ed., I. CRC Press, Taylor & Francis Group. https://doi.org/10.1201/9780429289774

Musse, M., Traore, A., Leca, A., Lahaye, M., Lorho, C., Pierre, G., ... Bertin, N. (2025). Insight into the mechanisms involved in the evolution of structural and physicochemical properties of tomato during air-drying - a study combining MRI imaging, unilateral NMR and conventional techniques. *Food Research International*. https://doi.org/10.1016/j.foodres.2025.116385

Orfila, C., Huisman, M. M. H., Willats, W. G. T., van Alebeek, G.-J. W. M., Schols, H. A., Seymour, G. B., & Knox, J. P. (2002). Altered cell wall disassembly during ripening of *Cnr* tomato fruit: Implications for cell adhesion and fruit softening. *Planta*, 215, 440-447. https://doi.org/10.1007/s00425-002-0753-1

Phyo, P., Wang, T., Xiao, C., Anderson, C. T., & Hong, M. (2017). Effects of pectin molecular-weight changes on the structure, dynamics, and polysaccharide interactions of primary cell walls of Arabidopsis thaliana: Insights from solid-state NMR. *Biomacromolecules*, 18(9), 2937-2950. https://doi.org/10.1021/acs.biomac.7b00888

Prothon, F., Ahrné, L., & Sjöholm, I. (2003). Mechanisms and prevention of plant tissue collapse during dehydration: A critical review. *Critical Reviews in Food Science and Nutrition*, 43, 447-479. https://doi.org/10.1080/10408690390826581

R Core Team. (2024). In In. (Ed.), *R: A language and environment for statistical computing v 4.4.1*. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-pr object.org.

Reynoud, N., Geneix, N., Petit, J., D'Orlando, A., Fanuel, M., Marion, D., ... Bakan, B. (2022). The cutin polymer matrix undergoes a fine architectural tuning from early tomato fruit development to ripening. *Plant Physiology*, 190(3), 1821-1840. https://doi.org/10.1093/plphys/kiac392

Rondeau-Mouro, C., Crepeau, M.-J., & Lahaye, M. (2003). Application of CP-MAS and liquid-like solid-state NMR experiments for the study of the ripening-associated cell wall changes in tomato. *International Journal of Biological Macromolecules*, 31, 235-244. https://doi.org/10.1016/S0141-8130(02)00086-7

Sinkora, M., Fanciullino, A. L., Bertin, N., Giovinzazzo, R., Zuber, F., Leca, A., ... Page, D. (2024). Variety, growing conditions and processing method act on different structural and biochemical traits to modify viscosity in tomato puree. *Food Research International*, 189, Article 114495. https://doi.org/10.1016/j.foodres.2024.114495

Toivonen, P. M. A., & Brummell, D. A. (2008). Biochemical bases of appearance and texture changes in fresh-cut fruit and vegetables. *Postharvest Biology and Technology*, 48(1), 1-14. https://doi.org/10.1016/j.postharbio.2007.09.004

Van Audenhove, J., Bernaerts, T., De Smet, V., Delbaere, S., Van Loey, A. M., & Hendrickx, M. E. (2021). The structure and composition of extracted pectin and residual Cell Wall material from processing tomato: The role of a stepwise approach versus high-pressure homogenization-facilitated acid extraction. *Foods*, 10(5). https://doi.org/10.3390/foods10051064

Wang, B., Li, Y., Lv, Y., Jiao, X., Wang, Z., He, Y., & Wen, L. (2023). Dehydration-rehydration mechanism of vegetables at the cell-wall and cell-membrane levels and future research challenges. *Critical Reviews in Food Science and Nutrition*, 1-17. https://doi.org/10.1080/10408398.2023.2233620

Wang, D., Yeats, T. H., Uluisik, S., Rose, J. K. C., & Seymour, G. B. (2018). Fruit softening: Revisiting the role of pectin. *Trends in Plant Science*, 23(4), 302-310. https://doi.org/10.1016/j.tplants.2018.01.006

Wang, T., & Hong, M. (2016). Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. *Journal of Experimental Botany*, 67(2), 503-514. https://doi.org/10.1093/jxb/erv416

White, P. B., Wang, T., Park, Y. B., Cosgrove, D. J., & Hong, M. (2014). Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. *Journal of the American Chemical Society*, 136 (29), 10399-10409. https://doi.org/10.1021/ja504108h